Biol. Rev. (2000), 75, pp. 191–251
Printed in the United Kingdom # Cambridge Philosophical Society
191
Conodont affinity and chordate phylogeny
PHILIP C. J. DONOGHUE", PETER L. FOREY#
and RICHARD J. ALDRIDGE$
" School of Earth Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK (p.c.j.donoghue!bham.ac.uk)
# The Natural History Museum, South Kensington, London SW7 5BD, UK (plf!nhm.ac.uk)
$ Department of Geology, University of Leicester, University Road, Leicester LE1 7RH, UK (ra12!le.ac.uk)
(Received 4 June 1999 ; revised 29 November 1999 ; accepted 29 November 1999)
ABSTRACT
Current information on the conodonts Clydagnathus windsorensis (Globensky) and Promissum pulchrum Kova! cs–
Endro$ dy, together with the latest interpretations of conodont hard tissues, are reviewed and it is concluded
that sufficient evidence exists to justify interpretation of the conodonts on a chordate model. A new
phylogenetic analysis is undertaken, consisting of 17 chordate taxa and 103 morphological, physiological and
biochemical characters ; conodonts are included as a primary taxon. Various experiments with character
coding, taxon deletion and the use of constraint trees are carried out. We conclude that conodonts are
cladistically more derived than either hagfishes or lampreys because they possess a mineralised dermal
skeleton and that they are the most plesiomorphic member of the total group Gnathostomata. We discuss
the evolution of the nervous and sensory systems and the skeleton in the context of our optimal phylogenetic
tree. There appears to be no simple evolution of free to canal-enclosed neuromasts ; organised neuromasts
within canals appear to have arisen at least three times from free neuromasts or neuromasts arranged within
grooves. The mineralised vertebrate skeleton first appeared as odontodes of dentine or dentine plus enamel
in the paraconodont\euconodont feeding apparatus. Bone appeared later, co-ordinate with the development
of a dermal skeleton, and it appears to have been primitively acellular. Atubular dentine is more primitive
than tubular dentine. However, the subsequent distribution of the different types of dentine (e.g.
mesodentine, orthodentine), suggests that these tissue types are homoplastic. The topology of relationships
and known stratigraphic ranges of taxa in our phylogeny predict the existence of myxinoids and
petromyzontids in the Cambrian.
Key words : Agnatha, Gnathostomata, cladistics, conodont, chordate, craniate, evolution, phylogeny,
vertebrate, skeleton.
CONTENTS
I. Introduction ............................................................................................................................
(1) Poly-, para- and monophyly of the Conodonta ................................................................
II. Soft tissue anatomy..................................................................................................................
(1) The head...........................................................................................................................
(2) The trunk..........................................................................................................................
(3) The tail .............................................................................................................................
III. Hard tissues .............................................................................................................................
(1) The histological debate .....................................................................................................
(2) Tissue types .......................................................................................................................
(a) Lamellar crown tissue .................................................................................................
(b) White matter ..............................................................................................................
(c) Basal tissue..................................................................................................................
(3) Relative growth of the tissues ...........................................................................................
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P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
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IV.
V.
VI.
VII.
VIII.
IX.
X.
XI.
(4) Hard tissue homologies .....................................................................................................
(a) Lamellar crown tissue .................................................................................................
(b) White matter ..............................................................................................................
(c) Basal tissue..................................................................................................................
(5) Conodont element growth.................................................................................................
(6) Histochemical studies ........................................................................................................
Phylogenetic analysis ...............................................................................................................
(1) Taxon sampling ................................................................................................................
(2) Character coding...............................................................................................................
(3) Character matrix...............................................................................................................
(a) Brain, sensory and nervous systems ............................................................................
(b) Mouth and branchial system ......................................................................................
(c) Circulatory system ......................................................................................................
(d) Fins and fin folds ........................................................................................................
(e) Skeletal .......................................................................................................................
(f) Physiological ...............................................................................................................
(g) Miscellaneous..............................................................................................................
(4) Results...............................................................................................................................
(a) Experimental analysis of the data set .........................................................................
(b) Cyclostome monophyly...............................................................................................
(c) Alternative hypotheses of chordate relationships ........................................................
(d) The effects of alternative interpretations of conodont anatomy and histology ...........
(e) Testing alternative hypotheses of conodont affinity....................................................
(f) Summary of conclusions drawn from experimental analyses of our data set..............
(5) Character changes.............................................................................................................
(a) General .......................................................................................................................
(b) Nervous and sensory systems ......................................................................................
(c) Skeleton ......................................................................................................................
Conodont affinity.....................................................................................................................
Directions for future research ..................................................................................................
(1) General..............................................................................................................................
(2) The origin of the Conodonta ............................................................................................
(3) Euconodont phylogeny......................................................................................................
(4) Histology ...........................................................................................................................
(5) Microevolution..................................................................................................................
(6) Conodont element function...............................................................................................
Revised classification ...............................................................................................................
Conclusions ..............................................................................................................................
Acknowledgements ..................................................................................................................
References................................................................................................................................
Appendix .................................................................................................................................
(1) Character diagnostics ........................................................................................................
I. INTRODUCTION
‘ The problem of the zoological affinities of this group
remains … one of the most fascinating and perplexing
problems of palaeozoology ’ (Rhodes, 1954, p. 419).
When Frank Rhodes wrote his article on conodont
relationships for Biological Reviews in 1954, conodonts
were known exclusively in the form of phosphatic
tooth-like microfossils of unknown or uncertain
affinity. The perception of conodonts is now very
different. The discovery of soft tissue remains (Briggs,
Clarkson & Aldridge, 1983 ; Mikulic, Briggs &
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Klussendorf, 1985 a, b ; Aldridge et al., 1993 ; Gabbott,
Aldridge & Theron, 1995) has resulted in a
revolution in our understanding ; we now know that
conodonts are a group of eel-shaped animals with
the phosphatic elements constituting a complex
feeding apparatus. Although the systematic position
of conodonts is still contentious, the diversity of
opinion has narrowed greatly. Just a year before the
first conodont fossil with preserved soft tissues was
found, Mu$ ller (1981) compiled a list of groups to
which conodonts had been attributed ; his list
includes at least three kingdoms and almost every
major animal phylum. The debate is now much
Conodont affinity and chordate phylogeny
more tightly constrained (see Aldridge, 1987 ;
Aldridge et al., 1993) and almost all authorities agree
that conodonts are chordates, although a few
workers still advocate a chaetognath affinity (e.g.
Kasatkina & Buryi, 1996 a, b, 1997). Among those
authors who accept a chordate assignment, however,
there is still controversy regarding the precise place
of the conodonts within the chordate clade.
To conduct a cladistic analysis involving both
chordates and chaetognaths is currently not feasible,
as the affinity of chaetognaths themselves is highly
contentious. Some authors suggest that they are best
placed as a sister-group to the vertebrates
(Christoffersen & Arau! jo-de-Almeida, 1994),
whereas others doubt even their deuterostome
affinity (Halanych, 1996 ; Nielsen, 1995 ; Nielsen,
Scharff & Eibye-Jacobsen, 1996). A relationship
between conodonts and chaetognaths was first
suggested by Rietschel (1973) and was resurrected
by Briggs et al. (1983) as one of the possible
interpretations consistent with the features of the
first known conodont with preserved soft tissues
(IGSE [British Geological Survey, Keyworth]
13822). This interpretation was more strongly
advocated by Bengtson (1983 b), and is supported by
Kasatkina & Buryi (1996 a, b, 1997). However, the
resemblances between conodont and chaetognath
anatomy are vague ; both are small and bilaterally
symmetrical, and both bear ray-supported fins, but
the caudal fin of conodonts is dorso-ventrally rather
than laterally disposed as in chaetognaths (contra
Kasatkina & Buryi, 1996 a). Furthermore, the Vshaped structures apparent in the trunk of conodonts
have no parallel in the musculature of chaetognaths,
although there is some resemblance to the ovaries of
some taxa [e.g. Pterosagitta draco (Krohn, 1853)].
The possibility remains that the taphonomic state
of specimens preserving conodont anatomy masks
similarities between the two groups, but, as no
taphonomic studies of chaetognaths have been
undertaken, this remains difficult to assess. Comparison of fossil conodonts with fossil chaetognaths is
limited by the rarity of fossil chaetognath specimens.
Amiskwia sagittiformis Walcott from the Middle
Cambrian Burgess Shale was originally described as
a chaetognath, but has been reinterpreted as a
possible nemertine (Conway Morris, 1977).
Paucijaculum samamithion Schram from the midPennsylvanian Francis Creek Shale of Illinois has
been similarly reassessed (Richardson 1982). More
recently, Kraft & Mergl (1989) have described a
more convincing candidate, Titerina rokycanensis from
the Lower Ordovician of Bohemia, which preserves
193
a bilaterally disposed grasping array in what is
interpreted as the cephalic region. A longitudinal
gut, possible ovaries and a laterally disposed raysupported caudal fin are also preserved. The overall
anatomy of T. rokycanensis is distinctly chaetognathlike and quite dissimilar to preserved remains of
conodonts.
The interpretation of early Cambrian conodontiform elements known as protoconodonts as the
grasping spines of chaetognaths (Szaniawski, 1982)
provides another possible line of evidence, if the
evolutionary sequence from protoconodonts,
through paraconodonts to euconodonts (the true
conodonts) proposed by Bengtson (1976 ; Fig. 1)
were sustained. This linkage was further emphasised
by Bengtson (1983 a, b) and Szaniawski (1987), who
noted that the hypothesis that chaetognaths and
(eu)conodonts shared a common ancestor did not
necessarily conflict with conodonts being closely
related to the chordates. Andres (1988) has also
suggested a reconciliation between the chordate and
chaetognath hypotheses of affinity, proposing chaetognaths as ancestors to euconodonts, which are in
turn ancestral to the vertebrates. This suggestion is
consistent with a close relationship between chaetognaths and chordates (Christoffersen & Arau! jo-deAlmeida, 1994 ; Cavalier-Smith, 1998 ; Hall, 1998),
but at odds with recent molecular and morphological
work which supports the view that chaetognath
affinity lies amongst the protostomes (Telford &
Holland, 1993 ; Philippe, Chenuil & Adoutte, 1994 ;
Wada & Satoh, 1994 ; Nielsen, 1995 ; Nielsen et al.,
1996 ; Halanych, 1996 ; Zrzavy! et al., 1998 ; current
evidence suggests that chaetognaths are closely
related to the nematodes and gnathostomulids,
possibly forming a monophyletic group, see
Littlewood et al., 1998). Until the affinities of
chaetognaths are resolved, the relative position of
conodonts and chaetognaths remains untestable,
and an apparent morphological gulf between protoconodonts and paraconodonts limits the applicability of the evolutionary model forwarded by
Bengtson (1976 ; Fig. 1).
Aldridge & Purnell (1996), in a review of the
debate, considered six competing hypotheses put
forward in the recent literature for the systematic
position of conodonts amongst the living chordates
(Dzik, 1995 ; Kemp & Nicoll, 1995 a, 1996 ; Peterson,
1994 ; Aldridge et al., 1986, 1993 ; Gabbott et al.,
1995 ; Janvier, 1995). Although most of these
hypotheses have been couched in cladistic terminology or expressed in the form of cladograms, not
one is the result of a numerical cladistic analysis.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
194
A
B
C
Fig. 1. Proto- (A), para- (B) and eucondont (C) grades of organisation (after Bengtson, 1976, and Szaniawski &
Bengtson, 1993). (A) Different shadings distinguish three layers which have no homologues in B and\or C. (B, C)
Dark shading represents basal tissue of euconodonts and its putative homologue in paraconodonts ; light shading
represents lamellar crown tissue of euconodonts.
Instead, each hypothesis represents the result of
placing conodonts in a pre-existing cladogram using
pre-established synapomorphies, or classifies them
according to unsubstantiated a priori assumptions of
character polarity in chordate phylogeny, or places
them within a phylogeny based on a consideration of
limited parts of the anatomy. This is unfortunate, as
conodonts clearly have an important contribution to
make to our understanding of chordate evolution.
Their significance centres around the feeding
elements, which represent the only biomineralised
component of the conodont skeleton. Depending on
whether conodonts are acraniate or craniate
chordates, their elements are either an interesting
but esoteric feature (in the former case), or an
important clue to the development of the mineralised
skeleton in craniate phylogeny (in the latter case).
The main aim of this contribution is to determine
the systematic position of the Conodonta through
formal cladistic analysis. To this end, we briefly
review interpretations of the anatomy and histology
of conodonts in order to explain our coding of
characters in the data matrix on which our analysis
is based. First, however, it is pertinent to consider the
monophyly of the Conodonta and to establish
precisely what constitutes a conodont.
(1) Poly-, para- and monophyly of the
Conodonta
Microscopic phosphatic cones, or ‘ conodontiform ’
fossils, first occur in the uppermost Precambrian and
become diverse in Cambrian strata. They were
divided into three main groups on histological
criteria by Mu$ ller & Nogami (1971, 1972) and
Bengtson (1976 ; Fig. 1). The stratigraphically oldest
group, the protoconodonts, are represented by
dominantly organic spine-like fossils which are
multilayered and grew by adding new layers to the
concave side of the elements only (Fig. 1 A).
Protoconodont elements bear a strong histological
resemblance to chaetognath grasping spines
(Szaniawski, 1982) and all available evidence indicates a probable link between these two groups
(Szaniawski, 1983, 1987). Paraconodont elements
are also relatively poorly mineralised ; in growth,
each successive phosphatic layer accreted onto the
margins and base, but not the tip of its predecessor
(Szaniawski & Bengtson, 1993 ; Fig. 1 B). These
elements bear a strong resemblance to the basal
body of euconodont elements (Lindstro$ m, 1964 ;
Bengtson, 1976). Euconodont elements are composed of two structures : the crown, which is very
heavily mineralised and relatively coarsely crystalline, and the basal body which is finely crystalline
and contains more organic material (Fig. 1 C). Both
components grew by external apposition of new
layers of mineral on the outer surface, which were
either added synchronously (Mu$ ller & Nogami,
1971) or at least in step (Lindstro$ m & Ziegler, 1971).
The lack of demonstrated links between protoconodonts and paraconodonts and the evidence that
the former are related to chaetognaths means that it
is likely that protoconodonts belong to a clade of
animals distinct from euconodonts (see also Peterson,
1994). An evolutionary link between paraconodont
and euconodont elements has been more firmly
a
id
Ozarkodinida
Pr
io
ni
od
on
tid
a
Prioniodinida
unnamed group
Panderodontida
unnamed group
?
Teridontus
Proconodontida
?
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nt
do
ro
de
an
op
ot
Pr
Paraconodontida
Conodont affinity and chordate phylogeny
?
Fig. 2. Attempted reconstruction of the relationships of the major groups of euconodont-grade taxa, based on the
suprageneric scheme and proposed relationships of Sweet (1988). This is not a cladogram but our interpretation of
the views expressed by Sweet (1988) in the form of a phylogenetic tree. The three orders of complex conodonts are
generally given equal taxonomic rank. However, it is implicitly accepted that the Ozarkodinida and Prioniodinida
are derived from taxa classified within the Prioniodontida. Therefore, we have chosen to express this relationship
explicitly in the figure and in the text.
established, primarily on the similarity in growth
pattern. Szaniawski & Bengtson (1993) have
attempted to demonstrate some transitional forms in
which layers of crown tissue were added to the basal
body only in late ontogeny. More recently, Mu$ ller &
Hinz-Schallreuter (1998) have documented the
histology of a number of Cambrian paraconodonts
which possess microstructural features comparable
with the basal tissue of euconodonts. The link
between paraconodonts and euconodonts points to
an origin for the whole group in the Early or Mid
Cambrian and renders the aptly named Paraconodontida a paraphyletic assemblage unless it is
expanded to include the Euconodonta. However,
monophyly of the Euconodonta is far from certain
and not all taxa currently regarded as euconodonts
necessarily fall within an inclusive Paraconodontida.
The early evolutionary history of the Euconodonta, or true conodonts, has been most clearly
documented by Miller (1969, 1980, 1984) who
distinguished two distinct lineages that are first
represented in the stratigraphic record by Proconodontus and Teridontus (Fig. 2). Both lineages are of
uncertain ancestry and both made their first appearance in the late Cambrian. The Proconodontus
lineage is known to have flourished in the Early
Ordovician but its subsequent evolution remains
unclear. The Teridontus lineage includes the overwhelming majority of conodonts and, although the
maximum diversity of this clade was also attained in
the Ordovician, it is known to have survived through
to the end of the Triassic Period. The three taxa
known with preserved soft tissue features all belong
to the Teridontus lineage, as do the vast majority of
taxa that have been studied histologically. Given the
uncertain and probable independent origins of
Proconodontus and Teridontus, we restrict our phylogenetic analyses of euconodonts to the monophyletic
lineage first represented by Teridontus.
II. SOFT TISSUE ANATOMY
The soft tissue anatomy of conodonts is known from
at least three euconodont taxa : Clydagnathus
windsorensis (Globensky) from the Lower Carboniferous Granton Shrimp Bed of Edinburgh, Scotland
(Aldridge et al., 1993) ; Panderodus unicostatus (Branson
& Mehl) from the Lower Silurian of Waukesha,
Wisconsin (Mikulic et al., 1985 a, b ; Smith, Briggs &
Aldridge, 1987), and Promissum pulchrum Kova! csEndro$ dy from the Upper Ordovician Soom Shale of
South Africa (Aldridge & Theron, 1993 ; Gabbott et
196
Fig. 3. For legend see opposite.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Conodont affinity and chordate phylogeny
al., 1995). There may be additional taxa represented
in the specimens from the Granton Shrimp Bed.
(1) The head
The most frequently preserved soft tissues are a
single pair of lobate structures, which occur commonly in association with natural assemblages of
conodont elements in the Soom Shale and are also
evident in two of the specimens from Granton. The
lobes occur as carbonised remains that are round to
oval in outline with a thickened or darker rim, and
have been reconstructed to three dimensions as a
pair of outwardly expanding cups (Aldridge et al.,
1993 ; Aldridge & Theron, 1993). From the Granton
specimens it is evident that these cups were located
slightly in front of and above the feeding apparatus
(Fig. 3 A–C). Aldridge & Theron (1993) drew
comparison with similar structures in the head of the
fossil jawless vertebrate Jamoytius kerwoodii White,
where they have been interpreted as eye capsules
(Ritchie 1968). Similar structures, interpreted as
traces of retinal pigments, have also been recorded in
a number of entirely soft-bodied fossil jawless
vertebrates including Myxinikela (Bardack 1991,
1998), Mayomyzon (Bardack & Zangerl, 1968, 1971)
and Hardistiella (Janvier & Lund, 1983 ; Lund &
Janvier, 1986). The most completely preserved
specimen of Promissum pulchrum (GSSA [Geological
Survey of South Africa, Pretoria] C721) includes
oval patches of white tissue in a similar position
relative to the feeding apparatus to that occupied by
the carbonised lobes in other specimens. This white
tissue has a fibrous texture comparable with
preserved muscle tissue in the trunk of the same
specimen, and was interpreted as extrinsic eye
musculature by Gabbott et al. (1995).
The interpretation of these structures as eye
capsules and eye musculature has been criticised by
Pridmore, Barwick & Nicoll (1997), who argued
that the paired lobes more probably represent otic
capsules. Pridmore et al. (1997) based their arguments on the size, shape and position of the lobes and
on an assertion that otic capsules are more likely to
be preserved in the fossil record than optic capsules.
However, size and shape are inadequate characters
197
to distinguish between otic and optic capsules (see
Donoghue, Purnell & Aldridge, 1998), and in
specimen IGSE 13821\2 from Granton, the lobes lie
anterior to a smaller pair of round structures which
have themselves been interpreted as otic capsules
(Aldridge et al., 1993 ; Aldridge & Donoghue, 1998 ;
Donoghue et al., 1998). There is, furthermore, no
evidence that otic capsules are more likely to be
preserved than optic capsules ; indeed, remnants of
eyes have been reported in all fossil representatives of
soft-bodied jawless vertebrates. In contrast, the
remains of unmineralised otic capsules are rare and
normally limited to moldic preservation (e.g.
Myxinikela ; Bardack, 1991).
The presence of extrinsic eye musculature in
specimen GSSA C721 is supported by evidence from
additional, recently discovered specimens of
Promissum pulchrum that also display paired lobes
composed of fibrous white clay minerals. Although
no other soft tissue remains are preserved in these
specimens, the lobate patches occur in consistent
topological association with natural assemblages of
elements, indicative of an original position above
and in front of the feeding apparatus. In a few
specimens, the patches are preserved only on the
part, but are matched by lobate traces of organic
film on the counterpart that are identical with the
structures interpreted as eye capsules on other
material. In extant lampreys, the extrinsic eye
muscles also match the eye capsules in their
distribution (see e.g. Fig. 3.6.I in Janvier, 1996 a).
Scanning electron micrography of the white patches
reveals a fibrous microstructure similar to the
preserved trunk musculature of specimen GSSA
C721 (Fig. 4 F–H).
In our codings for conodonts we have accepted the
growing evidence for the presence of extrinsic eye
musculature and we have taken the presence of
paired sensory organs (eyes and, perhaps, otic
capsules) to indicate the presence of a brain.
Specimen IGSE 13821\2 also shows faint traces of
approximately five paired rectangular box-like
structures posterior to the paired capsules (Fig. 3 A
in Briggs et al., 1983 ; Fig. 3 C). Each of these
structures is oriented with its long axis transverse to
the body axis. These compare well in shape and
Fig. 3. (A–E) Clydagnathus windsorensis (Globensky). (A, B) Part and counterpart of whole animal (respectively IGSE
13821 & 13822) ; frame widths 16 mm and 18 mm respectively. (C) Head region of part (IGSE 13821) ; frame width
25 mm. (D) Bilobed tail of IGSE 13821 ; frame width 7 mm. (E) Representative portion of the trunk (RMS GY
1992.41.1) ; frame width 10.5 mm. (A, C, D from Briggs et al. 1983 ; B, E from Aldridge et al. 1993). A, C, D are
reproduced from Briggs et al. (1983) with the permission of the Lethaia Foundation.
198
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Fig. 4. (A–H) Promissum pulchrum Kova' cs-Endro$ dy. (A, B) Part and counterpart of only known specimen preserving
trunk musculature (GSSA C721b, a respectively) ; frame widths 106 mm and 112 mm respectively. (C) Head region
including feeding apparatus and preserved extrinsic eye musculature (GSSA C721a) ; frame width 16 mm. (D, E)
Scanning electron micrograph of trunk musculature (GSSA C721a) ; D frame width 74 µm ; E frame width 22 µm.
(F–H) Extrinsic eye musculature under progressively higher magnification (GSSA C1320) ; F frame width 2900 µm ;
G frame width 930 µm ; H frame width 360 µm. B, D, E reproduced from Gabbott et al. (1995), with the permission
of Macmillan Magazines Ltd.
Conodont affinity and chordate phylogeny
position to gill pouches in the fossil lamprey
Mayomyzon (Aldridge & Donoghue, 1998), and in
our coding we follow Aldridge et al. (1993) in their
tentative interpretation of these structures as gill
pouches.
(2) The trunk
Trunk muscle tissues occur as distinct anteriorly
directed chevrons in the Granton specimens ; their
discrete nature is presumably the result of post mortem
decay and shrinkage, a process recognised in
decomposition experiments on Branchiostoma (Briggs
& Kear, 1994). The architecture of the muscle
blocks appears to be V-shaped, although the possibility remains that the myomeres were originally Wshaped with only the central V preserved (Donoghue
et al., 1998). In modern ammocoetes the myomeres
are W-shaped, but the dorsal limbs of the muscle
blocks are extremely short (P. C. J. Donoghue, pers.
obs.). Although there is some evidence for individual
fibre preservation in one of the Granton specimens
(RMS GY 1992.41.3 ; Aldridge et al., 1993) muscle
ultrastructure is best preserved in P. pulchrum (GSSA
C721), in which each myomere is demonstrably
composed of fibril bundles (Fig. 4 E), together with
possible sarcolemmic membranes and collagenous
connective tissues (Gabbott et al., 1995). This
specimen also includes a black organic patch within
the mid-trunk region that is probably the remains of
a visceral organ. Paired axial lines interpreted as the
margins of a notochord (Aldridge et al., 1993), run
the length of the trunk in all Granton specimens.
This interpretation has been corroborated by experimental decay of Branchiostoma, in which the
notochord decomposes to leave the notochordal
sheath, which then collapses to a pair of linear
thickened margins (Briggs & Kear, 1994). Remains
of a notochord have not been found in association
with Promissum pulchrum, but its position has been
considered to be represented by a 2 mm gap between
the dorsal and ventral limbs of the myomeres
(Gabbott et al., 1995). A possible nerve cord has been
identified stopping short of the paired lobes in two of
the Granton specimens (Aldridge et al., 1993).
(3) The tail
The tail is preserved in only two of the 10 specimens
from Granton, one of which (IGSE 13822) displays
an asymmetrical bilobed ray-supported fin. The fin
rays are closely set, without apparent branching,
and there is no evidence for supporting musculature.
Briggs et al. (1983) were unable to determine whether
199
the most extensive development of this fin was on the
dorsal or the ventral margin of the animal, but our
re-examination of IGSE 13822 indicates that the
bilobed portion occurs on the dorsal margin (Fig.
3 D). The second specimen (RMS [Royal Museum
of Scotland, Edinburgh] GY 1992.41.3) preserves an
unequally developed ray-supported fin that is longer
on the dorsal margin. The shape of the bilobed fin
compares to that of lampreys, where it is traditionally
interpreted as hypocercal. Janvier (1998) has recently compared the tail of RMS GY 1992.41.3 with
that of Myxine glutinosa, which he interprets as
cryptically hypocercal. Here, we regard the tail of
conodonts to be hypocercal because the bilobed fin is
restricted to the dorsal margin of the notochord, but
we do not accept Janvier’s (1998) argument as there
is no evidence of a ventral bend of the conodont
notochord at the caudal termination.
III. HARD TISSUES
The mineralised skeleton of conodonts is limited to
the phosphatic elements that are generally interpreted to have comprised a feeding apparatus. The
composition and architecture of this apparatus is
only fully understood for a few taxa, almost all of
which are highly derived, within the context of
conodont phylogeny as it is understood currently
(Fig. 2). We know very little of the apparatuses of
the earliest conodonts, with the simplest fully
reconstructed apparatus being that of Panderodus
which has cone-like elements of similar morphology
to those of primitive conodonts. The apparatus of
Panderodus was bilaterally arranged with eight pairs
of opposed elements and one symmetrical
‘ symphysial ’ element lying on the axis of symmetry
(Smith et al., 1987 ; Sansom, Armstrong & Smith,
1994). These elements are considered to have
performed a grasping function (Smith et al., 1987 ;
Sansom et al., 1994 a), although this hypothesis
remains to be tested.
More derived conodont groups typically possessed
elements of more complex morphology and their
apparatuses were composed from morphologically
distinct groups of elements. Almost all ‘ complex
conodonts ’ belong to the Prioniodontida and many
of these fall within the Ozarkodinida, the most
derived of all conodont groups (Fig. 2). The
architecture of non-ozarkodinid prioniodontids has
only been fully resolved for Promissum pulchrum,
which possessed nineteen elements, divided into four
pairs of robust ‘ P ’ elements which lay behind a pair
of ‘ M ’ elements, and above an array of ‘ S ’ elements
200
Fig. 5. For legend see opposite.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Conodont affinity and chordate phylogeny
comprising four pairs of asymmetrical elements and
a single, axial symmetrical element (Aldridge et al.,
1995). The function of this apparatus is not well
understood but S and M elements are interpreted as
having grasped prey (Aldridge et al., 1987) that was
sheared and crushed by the P elements prior to
digestion (Aldridge et al., 1995).
The apparatus of the most derived conodont
group, the Ozarkodinida, is known from several taxa
(see Purnell & Donoghue, 1998, for a review). The
ozarkodinids had sets of M, S and P elements, but, in
contrast to P. pulchrum, these units were arranged
linearly from rostral to caudal (Aldridge et al., 1987 ;
Purnell & Donoghue, 1997, 1998 ; Purnell,
Donoghue & Aldridge, 2000). Functional hypotheses
suggest that the S and M elements were used for
grasping, while a shearing and crushing function for
the P elements has been corroborated by studies of
microwear and functional morphology (Purnell,
1995 ; Donoghue & Purnell, 1999 b).
201
hard tissues of conodonts and vertebrates as homologues (Barskov, Moskalenko & Starostina, 1982 ;
Dzik, 1986 ; Burnett & Hall, 1992 ; Sansom et al.,
1992 ; Sansom, Smith & Smith, 1994 ; Sansom, 1996 ;
Smith, Sansom & Smith, 1996 ; Donoghue, 1998),
and those who seek to refute this hypothesis (Kemp
& Nicoll, 1995 a, b, 1996 ; Schultze, 1996).
(2) Tissue types
The crown of euconodont elements is either composed entirely from lamellar crown tissue, or includes
a core of opaque cancellous tissue known as white
matter. The basal body has also been interpreted as
a two-component structure (Gross, 1957, 1960), but
is currently regarded as a single tissue, termed basal
tissue by Donoghue (1998). Biomineralised basal
tissue is not preserved in the majority of postDevonian taxa, although pathological features in
some elements suggest that a basal body was present
in life (Donoghue, 1998).
(1) The histological debate
For the first 127 years of conodont research element
morphology and histology were the only clues to
affinity (for a review see Donoghue, 1998). Without
independent constraint over the phylogenetic position of conodonts, however, attempts at comparative histology proved futile. The discovery and
interpretation of soft tissue remains has now provided
a context within which conodont hard tissue histology can be assessed. Although there is a range of
opinion among those who have published histological results, recent contributors to the debate fall
clearly into two schools : those who interpret the
(a) Lamellar crown tissue
Within an element of any one taxon, lamellar crown
tissue exhibits a variable microstructure that is,
nevertheless, consistent between homologous
portions of homologous elements (Donoghue, 1998).
The crystallites that build the lamellae are typically
a few microns long but range from less than 1 µm to
more than 30 µm in length ; these layers of crystallites
are bounded at each end by incremental growth
lines (Fig. 5 B, C). In some of the taxa referred to the
Order Prioniodinida by Sweet (1988) the crystallites
are fibre-like in appearance, typically reaching 30
Fig. 5. Histology of conodont hard tissues. (A) Element of Coryssognathus dubius (Link & Druce) exhibiting the division
into crown and basal body ; (BU [Birmingham University, Lapworth Museum of Geology] 2616) ; frame width 547
µm. B,C. Lamellar crown tissue. (B) Horizontal section through a Pa element of Ozarkodina confluens ; (BU 2621) ; frame
width 78 µm. (C) Transverse section through a Pa element of Idiognathodus sp. ; (ROM [Royal Ontario Museum,
Toronto] 53261) ; frame width 124 µm. (D, G, H) Recurrent patterns of surface microwear compared to internal
discontinuities. (D) (ROM 49777) ; frame width 224 µm, inset element 698 µm in maximum length. (G) (ROM
49780) ; frame width 344 µm, inset element 1675 µm in maximum length. (H) (ROM 53445) ; frame width 352 µm.
(E, F) Basal tissue. (E) Tubular microstructure comparable to mesodentine in the Middle Ordovician Neocoleodus ;
(BU 2257) ; frame width 270 µm. (F) Globular and lamellar microstructure in Drepanodus from the Arenig of Estonia :
left frame in Nomarski differential interference, right frame in cross-polarised light ; (BU 2694) ; total frame width
250µm. (I, J) White matter. (I) Scanning electron micrograph of an etched section through a Pa element of Ozarkodina
confluens from the Upper Silurian of Gotland, Sweden ; (BU 2615) ; frame width 27 µm. (J) Pa element of O. confluens
immersed in optical oil demonstrating the relationship between white matter (the cancellar denticle core) and the
surrounding lamellar crown tissue ; (BU 2627) ; frame width 134 µm. (K, L) A natural pair of Idiognathodus Pa elements
dissected from the articulated skeletal remains of an individual conodont, articulated in the opposing extremes of their
occlusal cycle and viewed from the cauda ; (BU 2683) ; maximum length of dextral element 1182 µm. (M) Sc element
of Carniodus carnulus from the Lower Silurian of Estonia, immersed in optical oil and demonstrating the composite
nature of its struture ; (BU 2628) ; frame width 414 µm, maximum length of inset 890 µm.
202
µm or more in length with growth increments that
are only weakly discernible (Donoghue, 1998) ; the
arrangement of these fibres varies throughout individual elements.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
quently demonstrated that white matter and lamellar crown tissue share a common microstructural
fabric which, together with evidence of synchronous
growth suggests that both tissues are products of a
common developmental process.
(b) White matter
White matter is more finely crystalline than lamellar
crown tissue and is also distinguished by its albid
appearance in reflected light. The opacity of the
tissue results from the inclusion of small spaces (Fig.
5 I), ranging in size from less than 1 µm to more than
30 µm in maximum dimension. White matter is also
more resistant to etching agents than the enveloping
lamellar crown tissue (Stauffer & Plummer, 1932)
and as a result the distinction between the two tissues
becomes more obvious in etched sections. Despite
these differences, some specimens clearly demonstrate that these two tissues grew synchronously
(Donoghue, 1998 ; Fig. 5 J). The boundary between
the two tissues appears transitional in transmitted
light, but there is a sharp distinction between them
in etched section.
(c) Basal tissue
Basal tissue is the most variable of conodont hard
tissues. It almost always incorporates incremental
growth lines, but may be internally globular (Fig.
5 F), or tubular (Fig. 5 E), or globular and tubular,
or lacking in both globules and tubules (Donoghue,
1998).
(4) Hard tissue homologies
Given the evidence for conodont affinities based on
soft tissue anatomy, the hard tissues can now be
assessed within a chordate framework. Ascidiacean
and soberacean tunicates are capable of phosphatic
biomineralisation, but their spicules are homogenous
and composed of amorphous deposits or, in some
cases, dahllite. Extant myxinoids and lampreys
biomineralise phosphate in the form of statoliths
(Carlstro$ m, 1963) which are composed of an
amorphous (polyhydroxyl) form of calcium phosphate (Donoghue, 1998) ; these structures, again, do
not compare histologically with conodont elements.
There is some evidence that lampreys are capable of
endoskeletal biomineralisation (Bardack & Zangerl,
1971 ; Langille & Hall, 1993). In myxinoids, however, only the keratinous cap of the lingual teeth is
mineralised, and this mineralisation is limited to
isolated crystals embedded in a keratin matrix
(Dieckwisch & Vahadi, 1997). Although this may
prove to be of fundamental importance to our
understanding of the origin of teeth and of the
vertebrate dermal skeleton as a whole, it is not
possible to suggest primary homologies between the
mineralised hagfish teeth and the hard tissues of
conodonts.
(3) Relative growth of the tissues
Crown tissue is known to have grown by outer
apposition because many elements exhibit evidence
of damage and subsequent repair (Furnish, 1938 ;
Hass, 1941 ; Donoghue, 1998 ; Donoghue & Purnell,
1999 a ; Fig. 5 D, G, H). Incremental growth lines in
the lamellar crown and basal tissue meet at the basal
body-crown junction indicating that the two tissues
grew in synchrony (Mu$ ller & Nogami, 1971), and
hence basal tissue also grew by outer apposition. The
innermost core of any element therefore represents
the earliest growth stage, and the outermost the
latest. The two tissues grew in opposing directions
relative to the crown-basal body junction.
Donoghue (1998) used the architecture of the
putative cell and cell-process spaces in white matter
to argue that this tissue and lamellar crown tissue
had grown in synchrony, but in opposing directions.
However, Donoghue & Chauffe (1999) have subse-
(a) Lamellar crown tissue
The relatively coarse crystalline microstructure of
lamellar crown tissue shares no similarity with the
hard tissues of invertebrate chordates, even if we
consider the tissue in isolation (Donoghue, 1998).
The tissue is, however, closely comparable with
enamel and enameloid, the hypermineralised tissues
of vertebrate teeth and scales. The lamellar crown
tissue of the vast majority of conodont elements
compares most closely to enamel in its coarsely
crystalline microstructure and punctuating incremental growth lines (e.g. Fig. 5 B). It has been
suggested that the degree of microstructural variation apparent both within and between conodont
taxa, and even within an individual element, is
incompatible with an interpretation of this tissue as
an enamel homologue (Forey & Janvier, 1993). This
variation, however, coincides precisely with the
Conodont affinity and chordate phylogeny
requirements of element function and relates to the
different biomechanical forces that were imposed
upon the elements during feeding (e.g. Donoghue &
Purnell, 1999 b). Similar controls can be recognised
in the enamel microstructure of derived mammals
(v. Koenigswald, 1997), indicating that the enamel
of both mammals and conodonts was influenced by
analogous selective pressures (Donoghue & Purnell,
1999 b). Although by strict definition conodonts were
not teeth (Donoghue, 1998) they functioned in a
manner which is directly analogous (Purnell, 1995 ;
Donoghue & Purnell, 1999 a, b). The general lack of
complex enamels in lower vertebrates probably
reflects the fact that their teeth were not performing
complex occlusal functions. Some exceptions occur,
such as Uromastyx (the agamid lizard ; Cooper &
Poole, 1973) which has independently evolved
prismatic enamel in parallel with a complex occlusal
dentition. Similarly, sharks have independently
evolved a differentiated enameloid microstructure in
the dentitions of at least two distinct lineages, in
response to dental stresses (Reif, 1973, 1979, 1981 ;
Preuschoft, Reif & Mu$ ller, 1974).
(b) White matter
White matter has been the most controversial of all
the component hard tissues of conodont elements.
Sansom et al. (1992) interpreted it as cellular dermal
bone, but this is inconsistent with the growth interrelationship now recognised between lamellar crown
tissue and white matter (Donoghue, 1998). White
matter was secreted by the same cell population that
produced lamellar crown tissue (Donoghue &
Chauffe, 1999) and thus it can be neither a dentine
nor an enameloid tissue. It is more likely that white
matter was secreted by a slightly modified set of the
cells which secreted lamellar crown tissue. This
modification could have been effected by differentiation of the cells into a new type, by changing the
proximity of the secreting cells to the mineralising
front, or by the timing of secretion relative to other
members of the cell population. In any event, it is
now clear that white matter is autapomorphic to
some conodonts although developmentally homologous to enamel.
(c) Basal tissue
The basal tissue of various conodont taxa has been
compared to various dentines, types of bone and
calcified cartilage. However, no convincing evidence
has been presented for the presence of cell spaces and
203
a homology with bone is unlikely. A homology with
dentine is more sustainable, as the full range of
conodont basal tissues from lamellar atubular, to
tubular, to calcospheritic can be encompassed within
various dentine types (Donoghue, 1998). A plausible
argument has been presented for the presence of
globular calcified cartilage in the basal body of
Cordylodus angulatus (a member of the Proconodontus
lineage according to Miller, 1984) by Sansom et al.
(1992), through comparison with the endoskeletal
cartilage found in association with the dermal
skeleton of the Ordovician vertebrate Eriptychius
(Denison, 1967). The microstructure of the basal
tissue in C. angulatus, however, falls well within the
range exhibited by dentine (e.g. Plate 3 and Fig. 3 in
Sansom et al., 1997 ; see Donoghue, 1998). There is a
problem in resolving between the microstructures of
cartilage and dentine in fossils as small as conodont
elements, as features that might distinguish cartilage,
such as prismatic structure or an approximation of
it, occur in other taxa on a much larger scale.
However, examination of the calcospheritic structure
in the basal tissue of additional specimens of C.
angulatus and of Drepanodus arcuatus reveals that the
calcospheres often appear to have grown independently and are rarely enveloped within the
lamellae in the manner displayed by calcospheritic
dentines. The weight of evidence at present, therefore, indicates that one group of Lower Ordovician
conodonts (of the Proconodontus lineage) bore
elements partially composed from mineralised cartilage. Most basal tissues, however, are purely
lamellar and atubular, and resemble lamelin
(Donoghue, 1998), a form of dentine first described
from a Silurian chondrichthyan (KaratajuteTalimaa et al., 1990). In our coding, we recognise
that the major lineages of euconodonts have a basal
body composed of dentine, and regard the presence
of dentine as plesiomorphic for euconodont elements.
(5) Conodont element growth
Conodont elements grew in a manner directly
comparable to odontodes, the building blocks of the
vertebrate dermal skeleton (Donoghue, 1998). Each
element is reducible to a number of distinct
morphogenetic units, each composed from an individual crown and basal body (Donoghue, 1998).
These morphogenetic units were usually added
sequentially to the pre-existing, pre-formed structure. Internal discontinuities can be identified as
resulting from episodes of function alternating with
episodes of growth (Donoghue, 1998 ; Donoghue &
204
Purnell, 1999 a). Conodont elements performed a
tooth function while continuing to grow by marginal
addition of successive odontode generations in the
same manner as the dentigerous jaw bones of
acanthodians (Ørvig, 1973) and tooth plates of
lungfish (Kemp, 1977). More derived groups, such
as the ozarkodinids, must have undergone phases of
dormancy as successive odontodes were added
circumferentially, facilitating element repair. This
exaptation allowed the evolution of complex dental
mechanisms (Donoghue & Purnell, 1999 b).
The position of the elements within the mouth\
pharynx has led us to code pharyngeal odontodes as
present in conodonts, and conodont elements are
considered to be homologous to the pharyngeal
odontodes of both thelodonts and sharks.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
biochemical preservation is negligible. Furthermore,
the instability of collagen is such that it can only be
expected to survive biochemically for up to 1 million
years (see Aldridge & Purnell, 1996, and references
therein). Further cause for caution is raised by the
preparation of materials for histochemical analysis.
Picrosirius Red and comparable histochemical stains
for collagen are intended for use on fully decalcified
sections ; while Kemp & Nicoll (1995 a, b, 1996) used
decalcified sections of lungfish toothplates as their
control, the conodont elements were surface-etched.
An effect of the mineral salt in attracting the staining
molecule cannot be excluded in the interpretation of
their results.
IV. PHYLOGENETIC ANALYSIS
(6) Histochemical studies
Histochemical tests were first applied to conodont
elements by Fa/ hraeus & Fa/ hraeus-van Ree (1987,
1993), who used stains to investigate the insoluble
organic residues of decalcified specimens. The results
from these early studies were interesting but equivocal ; simple stained mounts of the organic films
revealed the presence of structures resembling
collagen fibres, although the source of the tissues
within the host elements was unknown. The approach has been refined by Kemp & Nicoll
(1995 a, b,1996) who extended the range of histochemical stains used and applied them directly to the
mineralised tissues. This technique produced positive
results for collagen in lamellar crown tissue, leading
Kemp & Nicoll (1995a, b, 1996) to reject the
hypothesis that this tissue is an homologue of enamel,
an entirely epithelial product lacking collagen.
White matter failed to stain for collagen and the
hypothesis that white matter is dermal bone was also
rejected because bone always contains collagen.
Kemp & Nicoll (1995 a, b, 1996) concluded that
conodont and vertebrate hard tissues are not
comparable. Their results also indicate the absence
of keratin, and the presence of cartilage ; they also
recorded a positive stain result for DNA in a Middle
Ordovician conodont element.
Attempts to repeat these results with modern and
fossil vertebrate hard tissues have failed (M.M.
Smith personal communication 1996 in Donoghue,
1998) and Kemp & Nicoll have also failed to
demonstrate the effectiveness of these tests on
undoubted fossil vertebrate material. Towe (1980)
has demonstrated that, although tissues like collagen
may be preserved physically with high fidelity,
Many commentators now accept the evidence for a
chordate affinity for conodonts, but the exact
position of the Conodonta within the Chordata
remains debatable (Aldridge & Purnell, 1996). To
date, only one attempt has been made to resolve the
systematic position of conodonts by formal cladistic
analysis (Janvier, 1996 b). This resulted in 79 equally
parsimonious trees, the strict consensus of which
placed conodonts in an unresolved position, but
more derived than either group of acraniate
chordates. Further runs of a modified matrix placed
conodonts as a sister-group of lampreys.
The phylogenetic analysis presented here considers representatives of a variety of lower craniate
taxa (Fig. 6), with the inclusion of Urochordata and
Cephalochordata as outgroups. Our data matrix is a
derivative of one compiled by P. Janvier & P. L.
Forey (in preparation) in which all characters were
entered in binary fashion (either a structure is there
or not), whereas we have opted to express some
characters as multistate entries ; the reasons for this
are explained below.
(1) Taxon sampling
The results of any phylogenetic analysis are subject
to the sampling of included taxa. Although this is a
particular problem with molecular data, where
single species are taken to represent large groups
(e.g. Xenopus laevis is usually taken as the representative of the Amphibia), it is also a concern
with morphological data. Here, two of the terminal
taxa cause us difficulty. For the Conodonta our
knowledge of soft tissue anatomy is limited to just
two species (Clydagnathus windsorensis and Promissum
Conodont affinity and chordate phylogeny
205
Fig. 6. Diagrammatic sketches of the terminal taxa used in our analyses. (A) Eptatretus stoutii (Lockington), a modern
hagfish (600 mm). (B) Petromyzon marinus Linneaus, a modern lamprey (800 mm). (C) Jamoytius kerwoodi White, a
naked anaspid-like fish from the Lower Silurian of Scotland (130 mm) ; K. A. Freedman (in press) has suggested that
there is absence of evidence for a dorsal and caudal fin in J. kerwoodi. (D) Clydagnathus windsorensis (Globensky), a
euconodont from the Lower Carboniferous of Scotland (60 mm). (E) Pharyngolepis oblongus Kiaer, a scaled anaspid
from the Upper Silurian of Norway (150 mm). (F) Errivaspis wayensis (White), a heterostracan from the Lower Devonian of England (150 mm). (G) Sacabambaspis janvieri Gagnier, an arandaspid from the Upper Ordovician of Bolivia
(after Gagnier 1989 ; 300 mm) – details of the tail are uncertain. (H) Furcacauda heintzae (Dineley & Loeffler), a deepbodied thelodont from the Lower Devonian of Canada (35 mm). (I) Hemicyclaspis murchisoni Egerton, an osteostracan
from the Lower Devonian of England (150 mm). (J) Loganellia scotica (Traquair), a thelodont from the Upper Silurian
of Scotland (120 mm). (K) Geraspis rara Pan & Chen, a galeaspid from the Middle Silurian of China – the tail is not
known in detail (150 mm). (L) Pituriaspis doylei Young, a pituriaspid from the Middle Devonian of Australia (headshield 45 mm in length).
pulchrum) and it is possible that these are not
representative of all conodonts (Panderodus unicostatus
from the Lower Silurian of Wisconsin, U.S.A., also
exhibits evidence of soft tissue remains although
these are too poorly preserved for adequate interpretation ; see Smith et al., 1987, and Conway
Morris 1989 a). However, C. windsorensis and P.
pulchrum scale a great taxonomic disparity but display
a similarity in preserved soft anatomy that suggests
that they can be taken as representative of the
monophyletic group Conodonta. This group is
characterised by phosphatic conodontiform elements
exhibiting a distinct crown composed of enamel and
a basal body composed of dentine ; as far as is known,
the body is laterally compressed with a short rostral
head portion in which the elements are located.
206
There is also evidence of a pair of rostro-lateral eyes
with extrinsic eye musculature, a pair of otic capsules
located caudo-medial to the eyes and, possibly, at
least four pairs of box-like gill pouches. The trunk is
elongate relative to its width, and constructed from
repeated symmetrical chevron-shaped muscle blocks
which are convex in a rostral direction ; the caudal
portion of the animal is dominated by an asymmetrically developed median fin supported by rays.
The fin is more extensive on the dorsal margin where
it is divided into two lobes.
Thelodonts are more problematic because of a
lack of agreement over their monophyly (e.g.
Turner, 1991, versus Janvier, 1981, for discussion).
Thelodonts are mostly represented in the fossil record
by isolated scales although some complete, articulated fossils are known. Thelodonts were characterised by Novitskaya & Turner (1998 : p. 533) as
having ‘ discrete dentinal scales with a base of
acellular bone-like tissue (aspidin) which is capable
of growth, and the production of simple to complex
anchoring devices ’. Most known articulated thelodonts are dorsoventrally flattened with asymmetrical
tails and with lateral flaps which lie above the gill
openings. However, the Furcacaudiformes are laterally compressed, possess a symmetrical tail and
lack lateral flaps ; they are nevertheless covered by a
micromeric dermal skeleton of thelodontiform scales
(Wilson & Caldwell, 1993, 1998). If thelodonts are a
monophyletic group, as advocated by Turner
(1991), it remains unclear which of the body shapes
is plesiomorphic. A phylogenetic analysis carried out
by Wilson & Caldwell (1998) placed dorso-ventrally
flattened thelodont genera in a polytomy with
gnathostomes, while Furcacaudiformes were
regarded as the monophyletic sister-group to this
combined group. If scale morphology is considered
as a more general character (e.g. if it is present in
galeaspids as suggested by Janvier, 1996b), then we
should either include both types of animal in our
cladistic analysis or simply select a single species\
genus with the proviso that this may not be
representative of all thelodonts. We have chosen to
adopt the latter course (selecting Loganellia as our
thelodont taxon) as we have not had the opportunity
to study for ourselves representatives of the Furcacaudiformes.
To justify the monophyly of other taxa included in
this analysis we have used the following criteria,
although these features are by no means exhaustive.
Hagfishes (Myxiniformes) show posterior displacement of the gill-pouch series and the presence of
slime glands. Lampreys (Petromyzontiformes) show
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
development of an oral sucker equipped with
denticles and the presence of a pharynx which is a
blind-ended diverticulum from the main tract of the
gut. Heterostracans are a large group of approximately 300 species of Lower Silurian to Upper
Devonian fishes, restricted to North America,
Europe and Siberia. They are characterised by a
single branchial opening covered by a single branchial plate associated with a large dorsal and ventral
shield. The most comprehensive and recent review of
the entire heterostracan group has been published
by Blieck (1984). In the present review, we assume
an internal phylogeny of heterostracans in which
forms such as traquairaspids represent the most
plesiomorphic condition. We have adjusted our
coding accordingly. For instance, we code the
presence of oak-leaf shaped tubercles as representative of heterostracans but we acknowledge that
such ornament is only found in our presumed
plesiomorphic representatives.
The Astraspida, Arandaspida and Eriptychiida
have traditionally been associated with the heterostracans on the basis of comparative histology.
However, since there is no clear consensus as to
which type of histology is plesiomorphic or
apomorphic and since discussion of histology is
central to this review we consider each of these taxa
separately.
Astraspis has been recovered from the Upper
Ordovician of North America, and exhibits an
armour constructed from small polygonal plates
composed of aspidin, orthodentine and enameloid.
There are separate branchial openings, each
associated with a small plate. Astraspis has been most
recently and most completely described by Sansom
et al. (1997).
The Arandaspida include the earliest-known fully
armoured craniates, Arandaspis from the Upper
Ordovician of Australia (Ritchie & Gilbert
Tomlinson, 1977), and Sacabambaspis from the Upper
Ordovician of Bolivia (Gagnier, 1993 a, b). The
arandaspids are characterised by large dorsal and
ventral shields, forward-looking eyes and a long
slanting series of rectangular branchial plates along
the flanks. The most comprehensive review of the
group was provided by Gagnier (1993 a, b).
Eriptychius is an enigmatic genus usually placed in
its own higher taxon (Eriptychiida), primarily
because its affinities are so poorly constrained. It is
known exclusively from fragments of dermal armour
which include tubercles composed of dentine and a
bony base underlain by globular calcified cartilage
(Denison, 1967). It has proven difficult to determine
Conodont affinity and chordate phylogeny
the precise systematic position of this taxon because
of the paucity of data available (see below).
The Osteostraci is the best-known group of
armoured jawless craniates ; approximately 300
species have been found in the Silurian and
Devonian of North America, Europe, Siberia and
Central Asia. Osteostracans possess a large semicircular dorsal head shield pierced by lateral and
median sensory fields, which are areas of small
tesserae connected to the labyrinth by means of bony
canals. The most comprehensive revision of the
group is that of Janvier (1985). Here, we accept
Janvier’s (1985) internal phylogeny for the group
which suggests that forms such as Ateleaspis and
Aceraspis, which possess pectoral fins, are plesiomorphic, and that the tremataspids, which lack
paired fins, are the most derived of osteostracans.
The Galeaspida (approximately 70 species
recovered from the Lower Silurian to the Upper
Devonian of China and North Vietnam) is a group
of craniates that superficially resemble osteostracans.
The dorsal surface of the head is covered by a single
broad and flattened head shield which is usually
semicircular in outline, but can be extended into
long cornuae and\or a long rostra in some taxa.
Galeaspid synapomorphies include a large, median
anterodorsal opening, interpreted as a nasohypophysial opening, and a unique scalloped pattern of
the main lateral-line canal upon the cephalic shield.
This group was most comprehensively reviewed by
Janvier (1996 a).
The Anaspida (approximately 25 species from the
Silurian to Upper Devonian of Europe and North
America) is a group of small fusiform fishes characterised by postbranchial scales or rods and a series of
elaborate mid-dorsal scales extending the length of
the body instead of a dorsal fin.
Jamoytius, Endeiolepis, Euphanerops and Legendrelepis
have traditionally been classified with anaspids but
lack both the modified postbranchial scales and middorsal scales typical of the Anaspida. Some authors
have considered one or more of these to be more
closely related to lampreys than to anaspids (e.g.
Forey & Gardiner, 1981, Arsenault & Janvier,
1991). Only the better known of these genera,
Jamoytius (Lower Silurian) and Euphanerops (Upper
Devonian) have been considered for the purposes of
the present phylogenetic analysis. Jamoytius has been
subject to very different interpretations (White,
1946 ; Ritchie, 1968 ; Forey & Gardiner, 1981), in
part because the preservation at the single known
locality is unusual. Recently, Jamoytius has been
restudied by K. A. Freedman (in press) and a great
207
deal of new information is now available both to
clarify ambiguities and to refute some aspects of
previous interpretations.
The Pituriaspida is represented by two species
from the Lower Devonian of Australia (Young,
1991) ; these are known only from natural moulds.
Although poorly known, they appear to have a solid
head shield perforated by large fenestrae immediately behind the eyes. We include them here because
the casts show some internal anatomy implying the
presence of bone and pectoral fins.
The Gnathostomata has always been recognised
as a monophyletic group whose Recent members
show many synapomorphies (Maisey, 1986), a few of
which may be listed as : primary upper (palatoquadrate) and lower (meckelian cartilage) jaws
which carry teeth erupting from a dental lamina ; a
supporting hyoid arch ; segmented branchial arches
lying internally to the blood and nerve supply and
the gill lamellae ; separate endoskeletal pectoral and
pelvic girdles and fin skeletons ; basals and radials
supporting dorsal and anal fins ; horizontal septum
dividing epaxial from hypaxial musculature ; horizontal semicircular canal ; myelinated nerve fibres ;
genitial ducts (Wolffian and Mullerian ducts)
developing from mesonephros ; renal portal system
and subcardinal veins. Some fossil gnathostomes
may lack some of these synapomorphies : for instance,
it is doubtful if placoderms had a dental lamina since
their dentition is non-replaceable.
For some of our characters gnathostomes are
polymorphic and thus an unambiguous coding may
depend upon an assumed phylogeny for basal
gnathostomes. There is little dispute that the
Chondrichthyes are the most plesiomorphic extant
gnathostomes and therefore we have opted to code
for the character states in this taxon. However, we
recognise that some workers accept that Placodermi
is the plesiomorphic taxon (e.g. Goujet & Young,
1995) and it is therefore possible that some codings
should be different. For instance, character 78 in our
data matrix refers to the condition of the dermal
head covering, which is micromeric in chondrichthyans and macromeric in most placoderms. For
each character where there is a potential dispute
over its coding in gnathostomes, we have discussed
and justified our scoring below.
(2) Character coding
As mentioned above we have used presence\absence
coding (Pleijel, 1995) in the majority of characters
but we have also used some multistate characters.
208
There is currently some debate about the usefulness
and theoretical underpinning of each of these
strategies (Pimental & Riggins, 1987 ; Pleijel, 1995 ;
Wilkinson, 1995 ; Hawkins, Hughes & Scotland,
1997 ; Forey & Kitching, in press) which may lead to
the establishment of different relationships.
Difficulty usually arises where some taxa do not
show a structure that others show in one or more
conditions. For instance, character number 18 relates
to the presence or absence of olfactory organs as well
as to the state of such organs, which may be paired
or unpaired. There are at least eight ways of coding
such observations (see Forey & Kitching, in press,
for discussion). Extreme presence\absence coding of
this character would code this as two columns of
data : 1. paired olfactory organs present or absent ; 2.
unpaired olfactory organs present or absent. This
means that taxa having no olfactory organs need to
be coded ‘ 0 ’ for both characters and the analysis
runs the risk of grouping taxa on the zero codings
(plesiomorphic long branch attraction). Also, it is an
assumption for the purposes of cladistic analysis used
here that each column of data provides potentially
independent evidence of relationship ; that is, the
columns are not linked biologically or logically. But
this is patently not so for the character under
discussion since the codings in one column predetermine the codings in adjacent columns. The
advantages of presence\absence coding are that it
maximises character congruence, reveals potential
homoplasy within the character and is the most
exacting test of homology.
Linking the observations into a single column as a
multistate character assumes that there is transformation between one observation and another and
denies the possibility that the evolution of unpaired
olfactory organs is independent of the origin of
paired olfactory organs. In this particular example,
it is possible that there may be no argument, since it
is known through ontogenetic studies of the lamprey
that the seemingly unpaired olfactory organ is a
transformation of the paired condition. But in linking
the nature of the dermal head covering (character
78 : absent, micromeric, macromeric) there is no
such ontogenetic evidence of transformation either
way and there may be a case for suggesting that
micromeric and macromeric are two independently
acquired expressions of a dermal skeleton.
An intermediate way of coding such characters is
the contingent coding method where one column of
data denotes the presence or absence of a structure
and the second column expresses the various conditions of that character with a ‘ not applicable ’
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
coding for those taxa which lack the structure.
Computationally, the ‘ not applicable ’ is coded as a
question mark. But this leads to further computational difficulties (Platnick, Griswold &
Coddington, 1991) such as the generation of multiple
equally parsimonious cladograms, many of which
contain spurious nodes.
At present there is no ‘ right ’ or ‘ wrong ’ way to
code for characters. We have chosen options that, to
us, make the most biological sense. But, as an
experiment we have recoded our data by translating
all the multistate characters to presence\absence
codings, and to contingent codings, and we have
used Sankoff coding which weights certain transformations (see below), to determine the effects on
the final topology.
(3) Character matrix
In this section, we list the characters, their possible
states and, where necessary, provide discussion of
how particular codes have been determined for
certain taxa.
(a) Brain, sensory and nervous systems
1. Neural crest. Absent l 0, present l 1. Inferred
from the presence of known neural crest derivatives
(e.g. dermal skeleton, gill arches, pigment cells). The
recording of neural crest in conodonts is based on the
presence of dentine and extrinsic eye musculature.
Smith, Graveson & Hall (1994) have proposed that
neural crest and epidermal placodes are derived
from a common phylogenetic precursor, while
Northcutt (1996 b) has subsequently provided preliminary evidence to suggest that neural crest and
epidermal neurogenic placodes have a common
developmental origin. It is possible, therefore, that
the presence of placode-derivatives may also be
taken for the presence of neural crest. As such, this
character partially overlaps with character 2 (brain)
which relies on the presence of paired sensory organs
for coding in many fossil taxa. Baker & BronnerFraser (1997) have recently argued for the presence
of neural crest precursors or putative homologues in
acraniate chordates based on : the presence of
AmphiDll- (the amphioxus homologue of Distal-less)
expressing migratory epidermis in amphioxus (Holland et al., 1996) which exhibits parallels to neural
crest in vertebrates ; the presence of dorsal sensory
neurons in the central nervous system of amphioxus
which may share a common origin with neural-crestrelated sensory neurons in the vertebrate CNS (e.g.
Conodont affinity and chordate phylogeny
mesencephalic nucleus of the trigeminal nerve ;
Narayanan & Narayanan, 1978) ; the presence of
putatively neurogenic migratory cells in tunicates
(Muske, 1993 ; Bollner, Beesley & Thorndyke, 1993,
1997 ; Bollner et al., 1995 ; Mackie, 1995) ; the
presence of mechanoreceptors in ascidian tadpoles
(Torrence & Cloney, 1982 ; Crowther & Whittaker,
1994), thaliaceans (Bone & Ryan, 1978) and
amphioxus (Bone & Best, 1978 ; Baatrup, 1981).
Baker & Bronner-Fraser (1997) even identify possible neural crest and placode precursors in nonchordate deuterostomes. However, neither precursors nor putative homologues can substitute for
the presence of neural crest and\or epidermal
placodes, and so we score this character as absent for
cephalochordates and tunicates.
2. Brain : absent l 0, present l 1. A brain here
is interpreted as an anterior enlargement of the
dorsal nerve chord which is morphologically differentiated and associated with one or more complex
sense organs (nasal sacs, paired and\or median eyes,
labyrinth) and cranial nerves with dorsal somatomotor roots and ventral visceromotor and viscerosensory roots. Garcia-Ferna' ndez & Holland (1994 ;
see also Holland & Garcia-Ferna' ndez, 1996) have
demonstrated that a portion of the cerebral vesicle
and dorsal nerve chord of Branchiostoma is homologous to the fore- and hindbrain of vertebrates.
More recently, Wada et al. (1998) have identified a
tripartite organisation to the neural tube of an
ascidian based on comparison between expression
patterns of Hroth, HrHox1 and HrPax-258 and their
homologues in vertebrates (Otx, Hox and Pax-2, -5,
-8, respectively). However, these are ‘ field ’ homologues rather than primary homologues and in
neither of the above cases do the fields give rise to
any clearly differentiated sensory organs [although
Wada et al. (1998) suggest that later expression of
HrPax-258 is associated with epidermal thickenings
(possible neurogenic placodes) which give rise to
what the authors suggest to be a homologue of the
vertebrate ear, and Sharman, Shimeld & Holland
(1999) describe the presence of placodes or placodehomologues in Branchiostoma]. There are no extant
craniates which show sensory organs and no brain.
Thus, it is assumed that evidence of any of the
sensory organs signifies the presence of a brain.
Direct evidence of the brain in fossil forms is seen as
endocasts of the brain cavity and is known in
osteostracans, galeaspids, and pituriaspids (Young,
1991). In conodonts, the evidence for the brain is
indirect ; in addition to the presence of paired
sensory organs, the notochord of conodonts (as
209
interpreted by Aldridge et al., 1993) appears to stop
short of the anterior end of the body (cf. Branchiostoma) and this may also indicate the existence of a
brain. It may also be pointed out that sensory
capsules etc. are also associated with a neurocranium
but in many of our chosen taxa there is no direct
evidence of this.
3. Olfactory peduncles. Absent l 0, present l
1. These are assumed to be present in heterostracans,
on the basis of the ridge leading from the pineal
recess to the nasal sac impressions, which corresponds
to the position of the olfactory peduncles observed in
galeaspids.
4. Pineal organ. Absent l 0, present and covered
l 1, present and uncovered l 2. In fossil forms, this
is usually indicated by a foramen or a depression on
the inner surface of the dermal skeleton. In Astraspis,
Sansom et al. (1997) have described a slightly raised
area of tesserae in the presumed position of the
pineal organ and this has been interpreted as
evidence of the presence of a pineal organ. A paired
pineal organ has been reported in the arandaspids
Arandaspis (Ritchie & Gilbert-Tomlinson, 1977) and
Sacabambaspis (Gagnier, 1993 a) and thus is coded
present here. However, it should be pointed out that
these paired openings lie well behind the eyes which
is an unusual position for such structures, and there
remains the possibility that these are paired endolymphatic openings. In hagfishes, there is no pineal
organ even though a habenular swelling and the
habenular ganglion are present (Wicht, 1996). As a
result, the presence of a habenular swelling in the
cranial endocast of pituriaspids (Fig. 6 in Young,
1991) does not constitute sufficient evidence for the
presence of a pineal organ. On structural evidence,
Lacalli, Holland & West (1994) and Lacalli (1996)
identified homology between the frontal eye and
lamellar body of Branchiostoma floridae and the paired
eyes and pineal organ (respectively) of vertebrates.
Again, this only demonstrates that the structures in
amphioxus and vertebrates are field homologues (cf.
Wicht, 1996). The expression of a Pax-6 homologue
(AmphiPax-6) in precursor cells of the frontal eye and
lamellar body in amphioxus (Glardon et al., 1998)
demonstrates only that a gene known to have a role
in the development of photoreceptors in a broad
range of animals (Callaerts, Halder & Gehring,
1997) is also implicated in photoreceptor development in amphioxus. Nevertheless, because of the
correlation between these two reports, we record ?
for this character in cephalochordates.
5. Pituitary divided to adenohypophysis and
neurohypophysis. Absent l 0, present l 1.
210
6. Adenohypophysis. Absent l 0, simple l 1,
segmented and compartmentalised l 2.
7. Optic tectum. Absent l 0, present l 1.
Ronan & Northcutt (1998) have recently described
an optic tectum in the brain of the Pacific hagfish
Eptatretus stouti.
8. Cerebellum. Absent l 0, present l 1. The
presence of a cerebellum in lampreys is usually
recorded. However, recent work (C. Weigle, personal communication ; Weigle & Northcutt, 1998)
suggests that the structure in lampreys cannot be
considered as a cerebellum since it lacks the auricles
which contain the emenentia granularis of
gnathostomes. The coding in fossil taxa showing
evidence of brain contours is based on the assumption
that the prominent paired swellings of the brain
cavity seen in heterostracans, osteostracans and
galeaspids (and possibly pituriaspids) are for the
cerebellum and not the optic lobes (see discussion in
Janvier, 1985).
9. Pretrematic branches in branchial nerves.
Absent l 0, present l 1.
10. Flattened spinal chord. Absent l 0, present
l 1.
11. Ventral and dorsal spinal nerve roots united.
Absent l 0, present l 1. Here, the hagfishes and
gnathostomes are coded the same ; that is, they both
have dorsal and ventral roots united. However, it
needs to be pointed out that in gnathostomes the
union lies immediately outside the dorsal nerve cord,
whereas in hagfishes the union lies deep within the
body musculature away from the nerve cord.
12. Mauthner fibres in central nervous system.
Absent l 0, present l 1.
13. Synaptic ribbons in retinal receptors. Absent
l 0, present l 1.
14. Number of nasal openings. None l 0, paired
l 1, single median l 2. The coding for heterostracans depends upon reconstruction of the grooves
that mark the undersurface of the snout as being
evidence of paired prenasal sinuses.
15. Nasohypophyseal opening serving respiration
(nasopharyngeal duct). Absent l0, present l 1.
16. Single nasohypophyseal opening. Absent l
0, present l 1.
17. Position of nasohypophyseal opening. None
l 0, terminal l 1, dorsal l 2.
18. Olfactory organ. Absent l 0, paired l 1,
unpaired l 2. Where an olfactory organ is present
the presence of a septum between the two halves of
the olfactory organ denotes a paired structure. Thus,
in Petromyzon fluviatilis there is a prominent median
septum dividing an outwardly median olfactory
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
organ (see Fig. 25 in Goodrich, 1909). This is taken
to indicate a paired ontogenetic origin.
However, it needs to be pointed out that
Gorbmann and Tamarin (1985) demonstrated that
in Petromyzon marinus the olfactory placode giving rise
to the olfactory epithelium is unpaired from the
beginning. It is therefore possible that lampreys are
polymorphic for this character. We have opted to
code lampreys as having paired olfactory organs on
the basis that other cranial sensory structures are
paired and hence, the plesiomorphic condition for
olfactory capsules is likely to be paired.
19. Extrinsic eye musculature. Absent l 0, present l 1. This is inferred in fossils from the presence
of myodomes and oculomotor nerve canals ; in
conodonts it is recorded on the basis of muscle fibres
preserved in intimate association with the organic
films interpreted by Aldridge & Theron (1993) as
eye capsules (e.g. Gabbott et al., 1995).
20. Presence\absence and number of semicircular
canals in labyrinth. None l 0, one l 1, two l 2,
three l 3. In heterostracans, there are clearly at
least two semicircular canals which appear to
correspond to the vertical semicircular canals of
gnathostomes, but since nothing is preserved other
than shield impressions it remains a possibility that
an horizontal semicircular canal was also present.
However, we note that the angle between the two
impressions for the vertical semicircular canals
appears to be marked by the impression for a gill
pouch (e.g. see Fig. 4.5A1 in Janvier 1996 a), which
would preclude the existence of a horizontal canal.
21. Vertical semicircular canals forming loops,
well separate from the vestibular division of the
labyrinth. Absent l 0, present l 1.
22. Externally open endolymphatic ducts. Absent
l 0, present l 1. For galeaspids, this is clearly
observed only in the genus Xiushuiaspis (Wang,
1991), but since this form is one of the most
plesiomorphic galeaspids (Janvier, 1996 a), the
character is assumed general for the entire group.
We have already commented upon the possibility of
endolymphatic ducts in arandaspids (see discussion
of character 4) but code here following the descriptions of the original authors.
23. Sensory-line system with neuromasts. Absent
l 0, present l 1. The presence of neuromasts is
assumed in fossils when sensory-line canals or long
continuous grooves are observed. Simple short or
irregular grooves are inconclusive, since such grooves
devoid of neuromasts exist in hagfishes. That the
grooves in hagfishes represent homologues of the
lateral line system of other craniates is supported by
Conodont affinity and chordate phylogeny
their development (Wicht & Northcutt, 1995),
innervation (Braun & Northcutt, 1997, 1998) and
central projections (Kishida et al., 1987). However,
the phylogenetic polarity of this condition (i.e.
primitive versus degenerate) is a moot point
(Fernholm, 1985 ; Wicht & Northcutt, 1995 ; Braun,
1996 ; Braun & Northcutt, 1997) ; as the sensory hair
cells are unoriented and lack cupulae, they are not
true neuromasts.
24. Electroreceptive cells. Absent l 0, present l 1.
25. Sensory-line grooves or canals. Absent l 0,
present on head only l 1, present on head plus body
l 2. The coding for Astraspida is based on the
recent description by Sansom et al. (1997), who
recorded the presence of paired short sensory grooves
confined to the pineal region of the head shield. It
has traditionally been observed that the lateral lines
of lampreys are restricted to the head. However,
Johnston (1905) documented the presence of lateral
lines continuing from head to trunk in Petromyzon,
and R. G. Northcutt (personal communication,
September 1999) records the presence of trunk
lateral lines in all genera of lampreys that he has
studied.
26. Sensory-line. Absent l 0, enclosed in grooves
l 1, enclosed in canals l 2. In some terminal taxa
used here sensory canals may be in grooves or canals
(e.g. osteostracans and galeaspids). Here, we record
the taxa as showing canals if any members have this
condition. Linking the condition of the lateral line
into a multistate character is justified by the
heterochronic relationship between the two states as
demonstrated for Ambystoma mexicanum by Northcutt,
Catania & Criley (1994).
(b) Mouth and branchial system
27. Pouch-shaped gills. Absent l 0, present l 1.
The presence of pouch-like gills signifies : the shape
of the openings as being pore-like ; that the gill
lamellae are inclined towards the centre of the gill
chamber in frontal section ; and the skeleton is
external to the lamellae. The pouch-like gill may be
round (lampreys and hagfishes) or transversely
elongated (some thelodonts, galeaspids and osteostracans). There is no known instance where the
opening is pore-like but the internal anatomy is like
the slit-like gills of gnathostomes (i.e. lamellae
inclined towards the opening and the skeleton medial
to the lamellae). Thus, the presence of pore-like
openings even in the absence of other knowledge (as
in arandaspids and anaspids) is assumed to indicate
a gill structure like that of lampreys and hagfishes.
211
The evidence for pouch-like gills in Eriptychius is
based on Ørvig’s (1958 : pl. 2, figs 4, 5) observation
of a branchial plate (incorrectly identified as a
branchio-cornual plate) with pore-like openings.
28. Gills alternate l 0, symmetrical l 1. In hagfishes, the gill pouches of either side alternate with a
corresponding alternation of the blood supply from
the ventral aorta. This may be an adaptation of an
eel-shaped body. However, a similar alternation of
the gills occurs in Branchiostoma and the condition
may, therefore, be plesiomorphic for craniates ; a
symmetrical distribution of the gill pouches on either
side of the midline would then be the derived
condition.
29. Elongate branchial series. More than 10 gill
pouches\slits l 0, fewer than 10 l 1. In Branchiostoma, there are numerous gill slits which extend well
down the body and this is accepted here as the
plesiomorphic craniate condition. The few but more
complexly developed gill pouches of most craniates
are regarded as derived. Some galeaspids, however,
have up to 40 branchial fossae. This is regarded here
as a derived state within this group, since all of the
most generalized galeaspids have fewer than 10 gill
openings or branchial fossae.
30. Gill openings lateral and arranged in slanting
row. Absent l 0, present l 1.
31. Position of gill openings. Gills opening laterally l 0, ventrally l 1.
32. Opercular flaps associated with gill openings.
Absent l 0, present l 1. This refers to a small
opercular flap, covered with minute dermal plates,
which partly covers the gill openings (e.g. in
osteostracans, thelodonts). These are presumed
absent when the gill openings are small, rounded,
and surrounded by solid dermal elements (e.g. in
arandaspids, astraspids, anaspids).
33. Endodermal gill lamellae. Absent l 0, present l 1.
34. Gill lamellae with filaments. Absent l 0,
present l 1. This is inferred in fossils when typical
gill lamellae impressions are observed.
35. Mouth terminal l 0 or ventral l 1. Our
coding for Jamoytius is taken from K. A. Freedman
(in press).
36. Velum. Absent l 0, present l 1.
(c) Circulatory system
37. Relative position of atrium and ventricle of
heart. Well separated l 0, close to each other l 1.
In fossils, the structure of the heart is only known in
212
osteostracans from the morphology of the pericardial
cavity (Janvier, 1985).
38. Closed pericardium. Absent l 0, present l 1.
39. Open blood system. Absent l 0, present l 1.
40. Paired dorsal aortae. Absent l 0, present l
1. This is inferred in some fossils from the shape of the
aortic groove. The condition within gnathostomes
does vary but here the presumed plesiomorphic
paired condition as represented in chondrichthyans
is coded.
41. Large lateral head vein. Absent l 0, present
l 1.
42. True lymphocytes. Absent l 0, present l 1.
43. Subaponeurotic vascular plexus. Absent l 0,
present l 1. This character is inferred to be present
in heterostracans, on the basis of the numerous
vascular grooves in Torpedaspis (Broad & Dineley,
1973), although most other heterostracans have a
smooth internal surface of the exoskeleton and show
no clear evidence of such a network. The subdermal
vascular canals of Eriptychius (Denison, 1967) are
assumed here to belong to this network. Sansom et al.
(1997) documented the presence of a canalised
network deep within the dermal armour of Astraspis.
We interpret this as a subaponeurotic vascular
plexus based on its similarity to the condition met
with in Eriptychius.
(d) Fins and fin-folds
44. Dorsal fin. Separate dorsal fin absent l 0,
present l 1. In cephalochordates and vertebrate
embryos, there is a continuous fin fold which extends
around the dorsal and ventral half of the body and
primitively continues ventrally in front of the cloaca
as the preanal fin fold. This initial fold is not
supported by any fin rays. In most adult vertebrates,
this fold becomes supported by radials and is
differentiated into separate dorsal, caudal and
sometimes anal fins : such differentiation is here
regarded as derived. In scaled anaspids such as
Birkenia and Pterygolepis etc. the dorsal margin of the
trunk is covered with modified and enlarged scales
which may be modifications of a dorsal fin, but since
there are no obvious signs of fin rays this group is
coded as lacking a dorsal fin. Our coding for
Jamoytius as having no dorsal fin is based on the
evidence provided by K. A. Freedman (in press).
45. Anal fin separate. Absent l 0, present l 1.
The primitive condition is taken to be a continuous
fin fold, with differentiation of a separate anal fin
being the derived condition. Here, there is assumed
to be no anal fin in osteostracans even though there
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
is a paired lateral fin fold developed at the base of the
tail in some taxa, such as Hemicyclaspis (Heintz,
1967).
46. Unpaired fin ray supports closely set. Absent
l 0, present l 1. In several fossil taxa (Heterostraci, Anaspida, Osteostracans and Thelodonti),
the ray supports are not observed directly, but their
position is inferred from the zonation of the
squamation.
47. Paired lateral fin folds. Absent l 0, present
l 1. This refers to any lateral or ventrolateral finlike fold, irrespective of whether they contain radials
and musculature. Hagfishes are coded here as
lacking such folds but it needs to be mentioned that
Jarvik (1980) has recorded the presence of lateral fin
folds in Neomyxine plicata. These structures are not
present in any other hagfish and N. plicata is not the
most plesiomorphic hagfish (Fernholm, 1998), therefore we regard these fin folds as non-homologous
with those developed in anapsids.
48. Constricted pectorals. Absent l 0, present l
1. This character refers to the gnathostome-like
postbranchial pectorals which have a constricted
base with an endoskeleton (cartilage or bone) and
associated musculature. No fossil jawless vertebrate
shows a clearly recognisable endoskeleton (although
some indication may be present in the Upper
Devonian Escuminaspis – Belles-Isles, 1989) but the
occurrence of musculature and possibly an endoskeleton is inferred in osteostracans and pituriaspids,
based on the scars and foramina inferred to be for
nerve\blood vessels left within the pectoral fenestra
of some species. To score osteostracans for this
character requires an internal phylogeny of osteostracans which proposes that Ateleaspis and Hemicyclaspis, which have well-developed pectoral fins,
are plesiomorphic osteostracans (see Janvier, 1985).
These deductions from the phylogenetic tree produced by Janvier (1985) echo earlier suggestions of
Stensio$ (1927) that tremataspids had lost paired fins,
and those of Heintz (1939) who considered that
Ateleaspis and Aceraspis are the most primitive
osteostracans.
49. Tail shape. Isocercal l 0, hypocercal l 1,
epicercal l 2. It is almost certain that the isocercal
tail is the plesiomorphic condition and evidence for
this may be seen in embryos of tail-bearing
vertebrates (ontogenetic criterion of character polarity), and in cephalochordates (outgroup
criterion). Both other conditions are here regarded
as equally derived and transformation between any
of the three is regarded as equally likely. Although
the position of the notochord is unknown in
Conodont affinity and chordate phylogeny
heterostracans, we opt here for an isocercal tail for
this group following descriptions by Denison (1971),
Soehn & Wilson (1990) and Wilson & Soehn (1990).
For Jamoytius, we have followed K. A. Freedman (in
press) who stated that the tail shape cannot be
reliably inferred from currently available specimens.
The tail of conodonts is scored as hypocercal for
reasons discussed above.
50. Preanal median fold. Absent l 0, present l
1. This character is extended to include the presence
of preanal scutes or crest in fossils possessing a
mineralised exoskeleton.
(e) Skeletal
51. Ability to synthesise creatine phosphatase. Absent l 0, present l 1. This function is assumed to
be present in all fossils having a skeleton made up of
calcium phosphate.
52. Visceral arches fused to the neurocranium.
Absent l 0, present l 1.
53. Horny teeth. Absent l 0, present l 1.
Ritchie (1960) noted denticles within the mouth
region of Jamoytius but did not describe their
composition. Re-examination of the material has
revealed that the structures in question are associated
with the naso-hypophysial opening and not the
mouth. Furthermore, identification of these structures as denticles is unlikely.
54. Trematic rings. Absent l 0, present l 1.
The series of ring-like impressions observed in
Jamoytius and Euphanerops are tentatively homologised with the trematic rings.
55. Arcualia. Absent l 0, present l 1. The presence of arcualia (neural arches and spines) is inferred
in osteostracans and heterostracans, which show
impressions of these structures on the undersurface of
the head shields (Janvier & Blieck, 1979), and in
galeaspids, which possess an elongated endoskeletal
occipital region which encloses the vagus nerve and
hence is inferred to include arcual elements.
56. Cartilaginous copula associated with tongue
protractor and retractor muscles. Absent l 0, present l 1.
57. Chondroitin 6-sulphate in cartilage. Absent
l 0, present l 1.
58. Braincase with lateral walls. Absent l 0,
present l 1.
59. Neurocranium entirely closed dorsally and
covering the brain. Absent l 0, present l 1.
60. Occiput enclosing vagus and glossopharyngeal. Enclosure of cranial nerves IX and X,
absent l 0, present l 1. In both hagfishes and
213
lampreys, the neurocranium extends back to enclose
the labyrinth within the otic capsule. In
gnathostomes, osteostracans, galeaspids and probably pituriaspids, it extends more posteriorly to
enclose both the glossopharyngeal and vagus nerves.
61. Annular cartilage. Absent l 0, present l 1.
This is best developed in the modern lamprey where
it supports the sucker. A comparable structure can
be seen in some fossil jawless vertebrates but there is
no direct evidence that a sucker was similarly
developed, nor that the preserved structure was
necessarily cartilaginous ; presence is scored for all
taxa with annular structures surrounding the mouth.
62. Trunk dermal skeleton. Absent l 0, present
l 1.
63. Perichondral bone. Absent l 0, present l 1.
Although pectoral fins are not always present in
association with perichondral bone (e.g. galeaspids),
the converse is true. Thus, we have been able to score
perichondral bone as present in pituriaspids even
though there is no record of histology. Further
evidence in support of this inference is supplied by
preservation of brain endocasts in pituriapids ; such
features could not be preserved in the absence of an
originally mineralised brain case.
64. Calcified cartilage. Absent l 0, present l 1.
65. Calcified dermal skeleton. Absent l 0, present l 1. The coding for conodonts is based on the
presence of calcified hard tissues forming the
elements. There is some dispute in the literature
concerning the presence of hard tissues in Jamoytius
(Ritchie, 1984 versus Forey & Gardiner, 1981).
Taphonomic studies by K. A. Freedman (in press)
indicate that Jamoytius possessed mineralised scales,
so we code the calcified dermal skeleton as present.
66. Spongy aspidin. Absent l 0, present l 1.
Although originally coined for a very specific tissue
type shown by pteraspids and psammosteids (Gross,
1930), the term aspidin now represents an unnatural
assemblage of histological types that are grouped
only by the presence of profuse fine fibre spaces.
While it is certain that not all these tissue types are
homologous, further classification requires a systematic study. We suggest that in future, the term
‘ aspidin ’ should be restricted to a tissue type that
incorporated aspidones. For this study we have
chosen to distinguish two types of ‘ aspidin ’ which
may not be mutually exclusive. Spongy aspidin
refers to tissue types which are alamellar and
incorporate aspidones.
67. Lamellar aspidin. Absent l 0, present l 1.
See notes for character 66 above. Lamellar aspidin
refers to tissue types that have traditionally been
214
interpreted as aspidin, but which lack aspidones and
are entirely lamellar.
68. Cellular bone. Absent l 0, present l 1. In
conodonts, we record cellular bone as absent for
reasons given in the text above.
69. Dentine absent l 0, mesodentine l 1, orthodentine l 2. Here, we classify dentine according to
the scheme of Ørvig (1967) where mesodentine refers
to a dentine in which the odontoblasts are enclosed
in the mineralised matrix and cell processes are
unpolarised. Orthodentine is typified by no cell
inclusion and parallel to sub-parallel, polarised cell
processes that are enclosed in the mineralised matrix.
The grouping of mesodentine and orthodentine into
a multistate character is justified by the evolutionary
relationship between these tissues, first proposed by
Ørvig (1967) and subsequently followed by Smith &
Hall (1990, 1993). While dentine is present in
conodonts (see above), it is neither mesodentine nor
orthodentine plesiomorphically ; we chose not to
introduce a further multistate for ‘ atubular dentine ’
because no other group in our analysis is known to
possess atubular dentine plesiomorphically and so
there is no potential homology. We have therefore
scored conodonts as ‘ ? ’ for this character.
70. Enamel\oid absent l 0, (monotypic) enamel
l 1, enameloid (bitypic enamel) l 2. Here, we
follow Smith (1989) in our distinction of enamel
(monotypic enamel) and enameloid (bitypic enamel). Grouping of the two tissues into a multistate
character is justified by their heterochronic relationship, as elucidated by Shellis & Miles (1974)
and subsequently followed by Smith (1989, 1992,
1995). Although the superficial glassy layer of
thyestidian dermal armour has traditionally been
interpreted as enameloid, the clear absence of
evidence for the presence of a basal lamina, and thus
an enameloid-dentine junction, precludes unequivocal interpretation of this tissue layer as such. Indeed,
it is equally likely that the superficial glassy layer in
thyestidian osteostracans is a hypermineralised dentine in which no tubules are present, resulting from
retraction of the cell processes prior to mineralisation
or from secondary backfilling of tubules. Furthermore, although this condition has traditionally been
extrapolated to typify the dermal histology of all
osteostracans, thyestidian histology is atypical and
derived.
71. Three-layered exoskeleton consisting of a
basal lamella, middle spongy (or cancellar) layer
and a superficial (often ornamented) layer. Absent
l 0, present l 1. Although it is not possible to
establish the exact nature of the dermal skeleton of
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
arandaspids this is known to be three-layered in at
least Sacabambaspis (Gagnier, 1993 a ; Young, 1997).
72. Cancellar layer in exoskeleton, with honeycombshaped cavities. Absent l 0, present l 1.
73. Composition of the scales\denticles\teeth.
Absent l 0, made up by a single odontode l 1,
made up by several odontodes l 2. Gnathostomes
are polymorphic for this character. Here, we accept
that the polyodontic scales of Palaeozoic sharks
represent the plesiomorphic state for gnathostomes.
74. Scale shape. Scale absent l 0, diamondshaped l 1, rod-shaped l 2. New observations of
Jamoytius suggest that there are rod-shaped scales
over the dorsal flank (K. A. Freedman, in press). The
primitive condition for the isolated scales in osteostracans is typified by Ateleaspis in which they are
diamond-shaped.
75. Oak-leaf-shaped tubercles. Absent l 0, present l 1. These are highly characteristic styles of
ornament which consist of elongated tubercles with
scalloped edges.
76. Oral plates. Absent l 0, present l 1. These
are found as either small parallel plates or larger
plates within the lower lip of some fossil forms. It is
thought that they were linked by soft tissue, so that
they could be extended as a scoop-shaped fan.
77. Denticles in pharynx. Absent l 0, present l
1. The coding for conodonts makes the assumption
that the conodont elements are homologous with
pharyngeal denticles in thelodonts and sharks.
However, it should be noted that the position of
conodont elements relative to the alimentary canal
remains unresolved and our contention that the
feeding apparatus occupied an oro\pharyngeal
position represents equivocation over whether it was
oral, pharyngeal or oropharyngeal in position.
78. Dermal head covering in adult state. Absent
l 0, small micromeric l 1, large (macromeric)
dermal plates or a shield l 2. The coding for
gnathostomes is debatable since they are polymorphic for this character. The plesiomorphic
gnathostome condition clearly depends on an
internal phylogeny and, more specifically the
relationships between placoderms (mostly macromeric) and chondrichthyans (micromeric) as well as
an internal phylogeny of placoderms. Recent literature (reviewed in Janvier, 1996 a) has settled on two
competing theories of relationships of placoderms
and other gnathostomes. Either they are the sistergroup of all other gnathostomes or they are the
sister-group of chondrichthyans. These theories lead
to ambiguity in polarising this character. Consideration of an internal phylogeny of placoderms
Conodont affinity and chordate phylogeny
similarly leads to uncertainty. More traditional
theories such as those of Denison (1978) suggest that
micromeric forms such as stensioellids are the most
plesiomorphic placoderms, in which case macromery
may have developed independently within the group
and, irrespective of the relationships as a group,
micromery would be plesiomorphic for gnathostomes. However, more modern theories include the
suggestions that stensioellids cannot be shown to be
placoderms (Janvier, 1996 a) and that other micromeric placoderms (radotinids) are not the most
plesiomorphic (Goujet & Young, 1995). Thus, we
are left with doubt. Because of this we disregard the
macromery of placoderms and accept that, since the
relationships of chondrichthyans to other living
gnathostomes is rarely in dispute, we should code the
plesiomorphic gnathostome condition as micromeric.
79. Large unpaired ventral and dorsal dermal
plates on head. Absent l 0, present l1.
80. Massive endoskeletal head shield covering the
gills dorsally. Absent l 0, present l 1. This refers
to the endoskeletal shield of galeaspids, osteostracans
and pituriaspids (inferred from the complex internal
casts).
81. Sclerotic ossicles. Absent l 0, present l 1.
These dermal elements which surround the eye are
present in a wide variety of gnathostomes but only
rarely seen in jawless vertebrates. Their presence in
arandaspids as recorded by Gagnier (1993 a) is
accepted here.
82. Ossified endoskeletal sclera encapsulating the
eye. Absent l 0, present l 1. Gagnier (1993 a)
describes a calcification around the eyeball of
arandaspids. Although there is some doubt about its
nature, this interpretation is accepted here.
( f ) Physiological
83. Blood volume. More than 10 % of body
volume l 0, less than 10 % of body volume l 1.
84. Haemoglobins with low O affinity and
#
significant Bohr effect. Absent l 0, present l 1.
85. Nervous regulation of heart. Absent l 0,
present l 1.
86. Heart response to catecholamines. Absent l
0, present l 1.
87. High blood pressure. Absent l 0, present l
1. Lampreys and gnathostomes show a considerably
higher basal metabolic rate and higher blood
pressures than hagfishes (Hardisty, 1979, 1982).
Indeed, the blood pressure of the hagfish is so low
that there are several regions of the circulatory
215
system where the walls of the blood vessels are
thickened, equipped with valves, and function as
accessory hearts.
88. Hyperosmoregulation. Absent l 0, present
l 1.
89. High proportion of serine and theronine
collagen. Absent l 0, present l 1.
90. Presence of lactate dehydrogenase 5. Absent
l 0, present l 1.
91. Pituitary control of melanophores. Absent l
0, present l 1.
92. Pituitary control of gametogenesis. Absent l
0, present l 1.
93. High metabolic rate. Absent l 0, present l
1. See Hardisty (1979, 1982) for discussion.
94. Ion transport in gills. Absent l 0, present l 1.
(g) Miscellaneous
95. Typhlosole in intestine. Absent l 0, present
l 1.
96. Spleen. Absent l 0, present l 1.
97. Collecting tubules in kidneys. Absent l 0,
present l 1.
98. Condensed and discrete pancreas. Absent l
0, present l 1.
99. A islet cells in the endocrine pancreas. Absent
l 0, present l 1.
100. Male gametes shed directly through the
coelom. Absent l 0, presentl 1.
101. Forward migration of postotic myomeres.
Absent l 0, present l 1.
102. Sexual dimorphism. Absent l 0, present l 1.
103. Larval phase. Absent l 0, present l 1.
Gnathostomes are assumed to have no larval phase
as the plesiomorphic condition.
(4) Results
‘ to some palaeontologists, fossils preserve information so
different from that derivable from living organisms that the
two cannot be classified in the same way. Surely the real
question is ‘‘ How much of this additional information is
essential to investigate a particular idea ?’’ ’ (Donovan &
Paul, 1998).
Parsimony analysis of the data presented in Table 1
resulted in three equally parsimonious trees, the
strict consensus of which is shown in Fig. 7 A. The
dataset was analysed using both PAUP 3.1.1
(Swofford, 1993) and Hennig86 (Farris, 1988),
which both produced the same topological results.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
216
A
Tunicata
B
Tunicata
Cephalochordata
Myxinoidea
Petromyzontida
Conodonta
Astraspis
Pituriaspida
Galeaspida
Osteostraci
Jawed vertebrates
Eriptychius
Loganellia
Euphanerops
Jamoytius
Anaspida
Arandaspida
Heterostraci
C
Tunicata
Cephalochordata
Myxinoidea
Petromyzontida
Pituriaspida
Galeaspida
Osteostraci
Jawed vertebrates
Eriptychius
Loganellia
Euphanerops
Jamoytius
Anaspida
Arandaspida
Heterostraci
Astraspis
Conodonta
Cephalochordata
Myxinoidea
Petromyzontida
10
100
Conodonta
6
99
Astraspis
2
53
Heterostraci
Arandaspida
2
58
Anaspida
Jamoytius
Euphanerops
Loganellia
Eriptychius
Jawed vertebrates
Osteostraci
Pituriaspida
Galeaspida
Fig. 7. (A) Strict consensus of the three equally most parsimonious trees ; 180 steps, CIe 0.654, RI 0.699, RC 0.458 ;
annotated nodes signify the Bremer Support (Clade Decay) value (top) and bootstrap value (bottom). Values are
only given for nodes with greater than one-step Bremer Support or greater than 50 % bootstrap support. (B) Strict
consensus of the 55 trees which are one step longer than the most parsimonious ; CIe 0.650, RI 0.694, RC 0.453. (C)
Strict consensus of the 459 trees which are two steps longer than the most parsimonious ; CIe 0.646, RI 0.689, RC
0.447.
The PAUP results are presented here (Fig. 7 A).
Multistate characters were left unordered and the
tree-building routine used was ie* implicit enumeration (Hennig86) or branch and bound (PAUP).
Tunicates and cephalochordates were used as a
paraphyletic outgroup but it should be stressed that
the topological results for the interrelationships of
craniates and conodonts are the same if either
tunicates or cephalochordates are used alone as the
outgroup. The same results were also obtained if a
consensus or monophyletic outgroup was used, and
in no instance did the results change after implementation of a posteriori reweighting (we used
retention index values). We also tried an all zero
ancestor as an outgroup taxon to explore the
possibility that conodonts might be resolved as the
sister-group to tunicates, but this also produced an
identical topology.
A number of comments are necessary about this
most-parsimonious solution. Most of the nodes on
this tree are supported by very few synapomorphies
(see Fig. 14) and two (under ACCTRAN optimisation) or four nodes (under the DELTRAN
optimisation) are supported entirely by homoplasy.
Furthermore, two frequently used measures of the
robustness of the tree – the bootstrap and Bremer
support (or clade decay) methods – imply weak
support for this topology (Fig. 7 A and Appendix).
The phylogenetic positions of two taxa, Eriptychius
and Pituriaspida, invite particular comment. Both
are very incompletely known (see Table 1) and the
high number of question marks introduces considerable uncertainty to the analysis.
Pituriaspids are here resolved in a trichotomy with
osteostracans and galeaspids. With ACCTRAN
optimisation applied to the character changes on the
three most-parsimonious trees this trichotomy is
supported by seven characters. There are five
homoplasies (involving characters 35, 45, 76–78)
among which pituriaspids are scored as ‘ ? ’ for three
(45, 76, 77). There are two synapomorphies, 31 and
80. Character 31 is coded as a question mark for
Conodont affinity and chordate phylogeny
217
Table 1. Data matrix of 17 chordate taxa. For descriptions of characters and state assignments see section IV(3).
Numbers to the right of the data matrix are percentage values of missing data for each of our operational taxonomic units.
‘ ? ’ against Recent taxa are due to non-applicable codings or codings where comparisons are of questionable primary
homology. Note that conodonts are not the most incompletely known taxa.
pituriaspids. Character 64 records the presence of a
massive endoskeletal head shield which covers the
gills dorsally, and our coding of ‘ 1 ’ for pituriaspids
is an inference from the complexity of the brain
endocast. Thus, in this analysis the only apparently
unambiguous support for the relationship of
pituriaspids with osteostracans and galeaspids is
based on inference.
Of the three possible resolutions to this trichotomy
the sister pairing of osteostracans and galeaspids
receives no support ; that is, it is a zero length branch
under the ACCTRAN optimisation. It is retained
because DELTRAN optimisation places characters
31 and 76 (both of which are ‘ ? ’ for pituriaspids) as
characters linking osteostracans and galeaspids. The
theory that pituriaspids and galeaspids are sister
groups is supported by changes in six characters (15,
32, 69, 71, 73, 82) all of which are homoplasies and
‘ ? ’ in pituriaspids. Finally, the grouping Osteostraci
jPituriaspida is supported by three homoplastic
character changes in states coded ‘ ? ’ for pituriaspids.
Therefore, the grouping of pituriaspids with osteostracans and galeaspids is at best questionable and at
worst disruptive in disguising synapomorphies between osteostracans and galeaspids which might
otherwise resolve a sister-group relationship between
these taxa. We have, therefore, undertaken another
analysis with pituriaspids excluded, and we have
chosen to depict the character changes on the single
resulting tree (see Figs 14 A, B, 15, 16).
Eriptychius has traditionally been placed close to
Astraspis, arandaspids and heterostracans, primarily
on the basis of common possession of spongy and
lamellar aspidin (the latter is also found in Loganellia
and galeaspids) ; its phylogenetic position in this
analysis as the sister-group of jawed vertebrates may,
therefore, appear radical. However, global parsimony resolves both attributes of aspidin as homoplastic. The sister-group relationship between
Eriptychius and jawed vertebrates in our most
parsimonious trees is supported by nine character
changes ; eight of these are homoplastic, six of which
are scored as ‘ ? ’ for Eriptychius (4, 14, 16, 17, 40, 52).
The other two are : character 69, which relates to the
acquisition of orthodentine (also seen in Astraspis and
heterostracans) and character 70, the acquisition of
(monotypic) enamel (also seen in conodonts). The
single synapomorphy linking Eriptychius and
gnathostomes (character 20) is coded as ‘ ? ’ for
Eriptychius. Similarly, the association of Eriptychius
with the clade containing gnathostomes, osteostracans and galeaspids is based on eight characters,
including a single synapomorphy which is unknown
in Eriptychius, and a further six homoplastic character
changes unknown for Eriptychius.
We cannot claim that the evidence for the
association of Eriptychius with gnathostomes in
particular or with the larger clade containing
gnathostomes, osteostracans and galeaspids in general is well supported. However, we have retained
Eriptychius within the tree listing character changes
because (a) its phylogenetic position is constant
among the three most parsimonious trees, (b) it does
not destroy the association between gnathostomes,
osteostracans and galeaspids and (c) histological
details of Eriptychius have traditionally played a
significant part in attempts to understand both the
interrelationships of ‘ agnathans ’ and the evolution
of the vertebrate skeleton.
The Bremer support values on our most-
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
218
A
Tunicata
B
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Myxinoidea
Petromyzontida
Petromyzontida
Conodonta
Conodonta
Anaspida
Astraspis
Jamoytius
Anaspida
Euphanerops
Jamoytius
Arandaspida
Euphanerops
Galeaspida
Loganellia
Pituriaspida
Eriptychius
Osteostraci
Jawed vertebrates
Heterostraci
Pituriaspida
Astraspis
Osteostraci
Loganellia
Galeaspida
Eriptychius
Heterostraci
Jawed vertebrates
Arandaspida
C
D
Tunicata
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Myxinoidea
Petromyzontida
Pituriaspida
Conodonta
Galeaspida
Euphanerops
Osteostraci
Jamoytius
Jawed vertebrates
Anaspida
Eriptychius
Eriptychius
Loganellia
Astraspis
Euphanerops
Heterostraci
Jamoytius
Arandaspida
Anaspida
Loganellia
Arandaspida
Galeaspida
Heterostraci
Jawed vertebrates
Astraspis
Pituriaspida
Conodonta
Osteostraci
Petromyzontida
Fig. 8. Effects of different ways of coding characters upon resolution and topology. In each case the strict consensus
tree is given with the numbers of fundamental trees, lengths, CIe – consistency indices (excluding uniformative characters), RI – retention indices, and RC – rescaled consistency indices. (A) presence\absence coding ; 9 trees, 199 steps,
CIe 0.585, RI 0.646, RC 0.386. (B) contingent coding ; 22 trees, 181 steps, CIe 0.638, RI 0.700, RC 0.456. (C) Sankoff
coding ; 10 trees, 185 steps, CIe 0.662, RI 0.713, RC 0.474. (D) Effect of deletion of all hard tissue characters ; 13007
trees, 125 steps, CIe 0.718, RI 0.735 and RC 0.529.
Conodont affinity and chordate phylogeny
parsimonious trees indicate how many extra steps
must be added before a particular node collapses.
It can be seen (Fig. 7 A) that with the exception
of the nodes subtending hagfishes and lampreys
with derived sister-groups most nodes are poorly
supported using this index. We also note that there
are many suboptimal trees at one step (Fig. 7 B) and
two steps (Fig. 7 C) longer ; therefore, the optimal
result is not strongly supported. However, the strict
consensus of the trees one step and two steps longer
show a range of included tree topologies fundamentally consistent with our most parsimonious
solution. More particularly, with respect to
conodonts, none of these trees is incongruent with
the classification (hagfishes (lampreys (gnathostomes
j conodonts))).
(a) Experimental analysis of the data set
Previous attempts at classifying agnathan fishes
(Forey & Janvier, 1993 ; Forey, 1995 ; Gagnier
1993 b, 1995) have all yielded results that are fragile
in the sense that individual nodes are poorly
supported. The possibility then remains that slight
changes in coding, taxon deletion\addition or choice
of outgroup may have severe consequences on the
phylogenetic hypothesis. To a very large extent the
fragility results from the difficulty expressed in our
epigram. Basically, modern agnathans are known
from only soft parts while the fossils are known only
from hard parts leading to the inclusion of many
question marks in the data matrix (see legend to
Table 1). The presence of large numbers of question
marks can generate many equally parsimonious
trees, including some that are spurious (that is, some
alternative nodes cannot be supported by any real
values which may be substituted for a question
mark). While we can lessen the effect of large
numbers of question marks we cannot eliminate the
basic problem, which resides with the fossils and not
with any particular method of analysis.
We have submitted our data set to a series of
experiments in order to test the robustness of the
data, to determine the effect that coding data in
different ways might have, to evaluate the effects of
the inclusion or exclusion of characters about which
the fossils are mute, and to address specific criticisms
regarding the inclusion of conodonts within a
chordate classification (e.g. Schultze, 1996).
Different ways of coding data embody different
theories of homology and may lead to different
phylogenetic outcomes (Pimental & Riggins, 1987 ;
Forey & Kitching, in press). In our data matrix, we
219
have 89 binary characters, most of which are
presence\absence codings. There are 14 multistate
characters, all but one of which are three-state
characters which usually describe the absence of a
feature plus two alternative states of that feature
(e.g. character 78, no head covering l 0, head
covering micromeric l 1, head covering macromeric l 2). This coding implies that there is a
transformational homology between the condition of
the head covering and does not allow for the
possibility they may be independent characters. One
radical alternative is extreme presence\absence
coding (Pleijel, 1995) where each separate observation is coded as a discrete character (character A,
micromeric head covering absent l 0, present l 1 ;
character B, macromeric head covering absent l 0,
present l 1). Recoding the data matrix in this way
results in 119 characters and nine trees, the strict
consensus of which is shown in Fig. 8 A ; the position
of conodonts relative to the extant chordates is
common to our original optimal trees. In this
particular analysis, a heuristic search was used,
employing 100 replicates of a random addition
sequence. It should be noted that major disadvantages of presence\absence coding are that
analyses of such matrices tend to overemphasise the
plesiomorphic attributes (the ‘ 0 ’ coding) and that
such coding fails to discriminate between primary
absence and secondary loss.
Another possible approach is to use contingent
coding (Hawkins et al., 1997), in which one character
expresses the presence\absence of the feature (e.g.
head covering), and another expresses the nature of
that feature (e.g. micromeric l 0, macromeric l
1), with those taxa lacking the feature scored as ‘ ? ’
(meaning not-applicable). Contingent recoding of
the multistate characters in our matrix results in 118
characters, analysis of which gives 22 equally
parsimonious trees (Fig. 8 B). Although many of the
taxa are placed in an unresolved polytomy, the
position of conodonts remains more derived than
hagfishes and lampreys but less derived than
armoured jawless vertebrates.
A third approach is to apply a priori weights to
certain character changes through the device of
Sankoff coding (Sankoff & Rousseau, 1975 ; Forey &
Kitching, in press). This type of coding applies a
‘ cost matrix ’ to the inference of character changes
that take place as the computer program is searching
for the most parsimonious tree(s). For example, we
may specify that to transform from no head covering
to micromeric costs one step, from no head covering
to macromeric costs two, from micromeric to
220
macromeric costs one and from either state of the
head covering to no head covering costs one.
Applying these types of step matrices to the eight
multistate characters for which they make potential
biological sense (characters 4, 17, 18, 25, 26, 69, 70,
78), analysis results in 10 equally parsimonious trees
with the strict consensus tree shown in Fig. 8 C. The
relationships remain largely compatible with our
preferred solution, with the position of conodonts
retained.
We also analysed the data set with all the
characters dealing with hard tissues deleted
(characters 46–67). 13007 equally most-parsimonious trees were found with the strict consensus tree
shown in Figure 8 D ; the lack of resolution underlines
the importance of hard tissue characters.
As a final experiment, we eliminated all of those
characters in which all fossils, including conodonts,
could only be scored as question marks (6, 9–13, 24,
33, 36, 38, 39, 42, 56, 57, 83–103). This tests for the
possible tendency of soft anatomical characters to
place lampreys as more derived than hagfishes.
However, the resulting topology was exactly the
same as our preferred result (Fig. 7 A) and we
conclude, therefore, that unavailability of soft tissue
characters in fossils is not affecting the ability of a
phylogenetic signal to come through (whether it is
correct is a different matter).
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
these results are equivocal : for example, although
the analysis of Lipscomb et al. (1998) of small subunit
(SSU) ribosomal RNA indicated cyclostome
monophyly when entire SSU ribosomal sequences
were analysed, when transversional changes of SSU
ribosomal sequences were analysed, the data
supported cyclostome paraphyly (see also Philippe et
al., 1994).
A large number of characters used in our analysis
can be identified a posteriori as synapomorphies
uniting lampreys and jawed vertebrates (and thus
separating hagfish and lampreys), but otherwise
contribute nothing to the resolution of relationships.
It could be considered, therefore, that our analysis is
an unfair test of cyclostome monophyly. To assess
this we conducted an analysis in which all but five of
these characters (6, 12, 13, 19, 20) were excluded
(characters 17, 23–25, 28–30, 34, 37–40, 42, 49, 50,
55, 57, 58, 83–99, 102 were excluded). The result of
a branch-and-bound analysis was three trees (strict
consensus shown in Fig. 9 A) which support cyclostome monophyly. Addition of a further synapomorphy (character 23) retained these three trees and
added a further three in which there is no support for
cyclostome monophyly ; the strict consensus of all six
trees is reproduced in Fig. 9 B. Addition of another
synapomorphy (character 24) resulted in the three
trees from our original analysis, exhibiting no
support for cyclostome monophyly.
(b) Cyclostome monophyly
Dume! ril (1806) first placed hagfish and lampreys
into a monophyletic group Cyclostomi (‘ rounded
mouth’) on the basis of two characters : a large
notochord and horny teeth. Through the work of
Cope (1889) the fundamental significance of the
presence and absence of jaws was first recognised
and the concept of a monophyletic Cyclostomata
persisted until the early 1970s. Subsequently,
Løvtrup (1977), Hardisty (1979, 1982) and a
number of other anatomists and palaeontologists
recognised that lampreys shared more derived
characters with jawed vertebrates than with hagfishes, and the Cyclostomata came to be regarded as
a paraphyletic group. However, molecular studies
have rekindled the concept of a monophyletic
Cyclostomata (Stock & Whitt, 1992 ; Lanfranchi et
al., 1994 ; Turberville, Schultz & Raff, 1994 ; Suzuki
et al., 1995 ; Mallatt & Sullivan, 1998 ; Lipscomb et
al., 1998), and Yalden (1985) and Mallatt (1997 a, b)
have both argued for cyclostome monophyly on
the basis of morphological characters (usually the
feeding apparatus and characters therein). Some of
(c) Alternative hypotheses of chordate relationships
Other authors have proposed very different patterns
of relationship from that which we derive here, and
we have selected four of these to act as backbone
constraint trees. The mutual relationships of the taxa
considered by the original authors were maintained
in each case while the remaining taxa were allowed
to establish their own relationships within this
framework (strictly, we used simple constraint trees
to represent previous hypotheses of relationships,
and taxa not included in previous analyses were
placed in an unresolved polytomy at the base of the
starting tree ; attempts at using conventional
backbone-constraint trees, in which only taxa considered by a previous author are included in the
constraint tree, failed due to the effect of numerous
synapomorphies stacked on the nodes separating
cephalochordates, hagfishes and lampreys). This
kind of experiment is in no way a test or criticism of
the original theories : two of the four trees (Fig. 10 A,
B) were not based on cladistic methods, all use only
Conodont affinity and chordate phylogeny
221
Fig. 9. (A) Cyclostome constraint tree ; 3 trees, 128 steps, CIe 0.614, RI 0.667, RC 0.411. (B) Cyclostome constraint
tree with synapomorphies removed ; 6 trees, 130 steps, CIe 0.612, RI 0.664, RC 0.409 ; (see text for discussion).
a subset of the taxa used in our analysis, none were
based on our data set, and three (Fig. 10 A–C) were
based on a much smaller and eclectic set of
characters. Thus, very little should be read into the
differing tree-lengths and other statistics. What is of
interest is that none of these analyses places
conodonts in our favoured position ; within the
constrained analyses conodonts are resolved as either
stem-craniates or stem-vertebrates. We interpret this
to suggest that the phylogenetic position of conodonts is dependent upon the phylogenetic relationships of other chordates and so, if we assume different
hypotheses of relationship amongst non-conodont
chordates, the phylogenetic position of conodonts is
very differently resolved. Thus, to place conodonts
into an existing chordate classification as a means of
explaining character evolution and the phylogenetic
significance of conodonts, it is first necessary to
justify the choice of chordate phylogeny. All previous
studies (e.g. those cited in Fig. 4 of Aldridge &
Purnell, 1996), bar that of Janvier (1996 b), have
failed to do this.
If there were several unambiguous synapomorphies which linked conodonts with one or
another terminal taxon (e.g. cephalochordates), the
differing theories of chordate relationships would
probably have little effect on our understanding of
the phylogenetic significance of conodonts. However,
in the absence of such strong phylogenetic signals we
conclude that the relationships (and hence the
significance) of conodonts cannot be established
independently of a theory of relationships of
chordates including conodonts. Furthermore, the
effect of exclusion of conodonts from our analysis
(Fig. 11 A) demonstrates that the unique suite of
chordate characters expressed by conodonts has
great significance for our understanding of chordate
phylogeny.
(d ) The effects of alternative interpretations of conodont
anatomy and histology
Although we contend that homology between
conodont and vertebrate hard tissues is wellfounded, several authors have expressed doubts (e.g.
Forey & Janvier, 1993 ; Kemp & Nicoll, 1995 a, b,
1996 ; Schultze, 1996 ; Pridmore et al., 1997). For this
reason we have undertaken analyses with all the
histological characters set to question marks against
conodonts. As a separate experiment, we have also
set the presence of eye muscles to a question mark, to
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
222
A
B
Tunicata
Tunicata
Cephalochordata
Cephalochordata
Heterostraci
Conodonta
Myxinoidea
Arandaspida
Conodonta
Astraspis
Jamoytius
Galeaspida
Euphanerops
Pituriaspida
Arandaspida
Eriptychius
Osteostraci
Jawed vertebrates
Petromyzontida
Jamoytius
Anaspida
Euphanerops
Pituriaspida
Loganellia
Galeaspida
Heterostraci
Loganellia
Myxinoidea
Jawed vertebrates
Anaspida
Astraspis
Petromyzontida
Eriptychius
Osteostraci
C
D
Tunicata
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Conodonta
Conodonta
Pituriaspida
Pituriaspida
Eriptychius
Arandaspida
Euphanerops
Euphanerops
Jamoytius
Eriptychius
Myxinoidea
Jawed vertebrates
Petromyzontida
Loganellia
Osteostraci
Heterostraci
Galeaspida
Astraspis
Arandaspida
Osteostraci
Astraspis
Galeaspida
Heterostraci
Petromyzontida
Anaspida
Anaspida
Jawed vertebrates
Jamoytius
Loganellia
Fig. 10. Result of incorporating backbone constraint trees (bold lines) based upon existing hypotheses of relationships.
(A) Stensio$ (1968) constraint tree ; 1 tree, 215 steps, CIe 0.547, RI 0.527, RC 0.290. B. Moy-Thomas & Miles (1971)
constraint tree ; 2 trees, 248 steps, CIe 0.474, RI 0.369, RC 0.176. C. Halstead (1982) constraint tree ; 1 tree, 206
steps, CIe 0.571, RI 0.573, RC 0.328. D. Gagnier (1995) constraint tree ; 9 trees, 209 steps, CIe 0.562, RI 0.558, RC
0.315.
Conodont affinity and chordate phylogeny
test the contentions that conodonts are resolved as
vertebrates through assumed homologies of the hard
tissues and eye muscles (Kemp & Nicoll, 1995 a, b,
1996 ; Schultze, 1996 ; Pridmore et al., 1997). These
experiments produced identical results (Fig. 11 B),
with conodonts again resolved as cladistically more
derived than lampreys. Setting the character codings
for the same characters to ‘ 0 ’ instead of ‘ ? ’ for
conodonts produces an identical consensus tree.
Thus, even if we claim that the histological structures
in conodonts and the conodont eye muscles are
definitely not those of vertebrates, conodonts are still
resolved as more derived than lampreys. The
synapomorphy supporting this position in this case is
the presence of a mineralised dermal skeleton
(character 65). Conodont hard tissues have been
recognised as dermal at least since the work of Gross
(1957, 1960), an hypothesis that has not been
disputed. Nevertheless, if we experiment with this
coding by scoring ‘ ? ’ for the presence of a dermal
skeleton, ‘ ? ’ for the presence of specific hard tissues,
and ‘ ? ’ for the presence of extrinsic eye musculature
in conodonts, parsimony analysis results in 48
optimal trees in which the relationship between
conodonts and lampreys is unresolved (Fig. 11 C). If
these codings are all changed to ‘ 0 ’ for conodonts,
parsimony analysis identifies 42 optimal trees, the
strict consensus of which places conodonts below
lampreys and above hagfishes (Fig. 11 D).
(e) Testing alternative hypotheses of conodont affinity
Despite the limited data, conodonts have been
interleaved in almost every possible permutation
with the major groups of living chordates. To
compare the results of our analysis with the various
previous hypotheses we have re-analysed our data
set enforcing topological backbone constraint trees
representing each hypothesis.
In discussing the affinity of Yunnanozoon, Dzik
(1995) proposed that conodonts are more primitive
than all the living chordates. Assessing this hypothesis is problematic as it necessitates moving
Tunicata and Cephalochordata to the in-group ; for
the purposes of this experiment we have adopted an
all-zero outgroup. Branch-and-bound analysis
identified 42 most-parsimonious trees at 192 steps
with a topology meeting the requirements of the
backbone constraint tree (Fig. 12 A), in contrast
with the 180 steps in our optimal tree (Fig. 7 A).
However, this is not necessarily an adequate test of
how Dzik’s (1995) hypothesis of conodont affinity
compares to our preferred hypothesis, as he con-
223
sidered Tunicates and Cephalochordates to be more
closely related to each other than either group is to
conodonts, hagfish or lampreys. We conducted a
further analysis incorporating this constraint ; the
result is 42 most-parsimonious trees at 193 steps with
a topology meeting the requirements of the backbone
constraint tree (Fig. 12 B). In both instances, the
topology of the strict consensus tree is the same (Fig.
12 A).
Kemp & Nicoll (1995 a, 1996) proposed that
conodonts are more closely related to the cephalochordates than to any other group of chordates.
Analysis of the data set while enforcing a backbone
constraint tree compatible with this hypothesis
produces 42 equally most-parsimonious trees at 190
steps (Fig. 12 C).
Both Peterson (1994) and Pridmore et al. (1997)
suggested that conodonts might best be positioned as
a sister-group to the Craniata. 45 trees at 186 steps
are identified as the shortest compatible with their
hypothesis (Fig. 12 D). Krejsa, Bringas & Slavkin
(1990 a, b) argued that conodonts and hagfish are
more closely related to each other than either is to
any other group based largely upon putative
homology between conodont elements and hagfish
toothlets. A branch-and-bound search found 45 trees
at 186 steps as the shortest compatible with this
hypothesis ; a strict consensus is shown in Fig. 13 A.
The hypothesis of conodont affinity commonly
preferred by workers on non-skeletal remains places
conodonts as a sister group to the lampreysjjawed
vertebrates (Aldridge et al., 1986, 1993 ; Aldridge &
Briggs, 1986 ; Aldridge, 1987 ; Aldridge & Purnell,
1996 ; Aldridge & Donoghue, 1998 ; Donoghue et al.,
1998). 45 trees at 182 steps are identified as the
shortest compatible with this hypothesis ; a strict
consensus of all appears in Fig. 13 B. Alternatively,
Janvier (1996 b) has proposed that conodonts and
lampreys are sister-taxa ; we found three trees at 182
steps as equally most-parsimonious compatible with
this constraint topology (Fig. 13 C). The topology of
the strict consensus tree is otherwise common to the
strict consensus of the three optimal trees generated
without a backbone constraint (Fig. 7 A). Janvier
(1995) has also proposed that conodonts might be
more closely related to a group including the
Osteostraci, Pituriaspida and crown-group gnathostomes, based upon a possible homology between
conodont white matter and mesodentine\cellular
dermal bone. Branch-and-bound search identified
six trees at 187 steps as the shortest compatible with
the enforced backbone constraint tree ; the topology
of a strict consensus is shown in Fig. 13 D).
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
224
A
Tunicata
B
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Myxinoidea
Petromyzontida
Petromyzontida
Anaspida
Conodonta
Astraspis
Jamoytius
Heterostraci
Euphanerops
Arandaspida
Loganellia
Anaspida
Eriptychius
Jamoytius
Jawed vertebrates
Euphanerops
Pituriaspida
Loganellia
Osteostraci
Eriptychius
Galeaspida
Jawed vertebrates
Astraspis
Osteostraci
Heterostraci
Pituriaspida
Arandaspida
Galeaspida
C
D
Tunicata
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Myxinoidea
Conodonta
Conodonta
Petromyzontida
Petromyzontida
Anaspida
Anaspida
Jamoytius
Jamoytius
Euphanerops
Euphanerops
Loganellia
Loganellia
Eriptychius
Eriptychius
Jawed vertebrates
Jawed vertebrates
Pituriaspida
Pituriaspida
Osteostraci
Osteostraci
Galeaspida
Galeaspida
Astraspis
Astraspis
Heterostraci
Heterostraci
Arandaspida
Arandaspida
Fig. 11. (A) Effect of exclusion of conodonts from the analysis ; 42 trees, 178 steps, CIe 0.661, RI 0.703, RC 0.466.
(B) Effect of changing conodont histological characters and the eye muscle character to question marks (a number of
separate analyses all resulted in the same topology, but with slightly different statistics) ; 3 trees, 178 steps, CIe 0.661,
RI 0.706, RC 0.468. C. Effect of changing all histological characters, extrinsic eye musculature and ‘ dermal skeleton ’
in conodonts to ‘ ?’ ; 48 trees, 178 steps, CIe 0.661, RI 0.706, RC 0.468. D. Effect of changing all histological characters, extrinsic eye musculature and ‘ dermal skeleton ’ in conodonts to ‘ 0’ ; 42 trees, 178 steps, CIe 0.661, RI 0.710,
RC 0.471.
Conodont affinity and chordate phylogeny
( f ) Summary of conclusions drawn from experimental
analysis of our data set
The results of our phylogenetic experiments show
that conodonts are consistently placed within vertebrates and that, with the exception of one type of
coding (substituting ‘ 0 ’ for eye muscle and all
histological characters in conodonts) the results are
consistent with the proposition that conodonts are
cladistically more derived than lampreys, that is :
they are basal members of the Gnathostomata. In
commentary on the epigram to this section we would
suggest that the presence of ‘ V ’-shaped myotomes
and paired sensory organs place conodonts within
the Chordata but that the extra information required
to place them more accurately centres on interpretation of conodont elements as part of a mineralised
dermal skeleton.
(5) Character changes
(a) General
The topology of our most-parsimonious tree (Fig.
7 A) is very similar to the results of other recent
phylogenetic analyses of primitive vertebrates. As
such, the implications of character changes for the
phylogeny of many organ systems differ little from
these publications, and in these instances we direct
the reader to the work of Forey & Janvier (1993),
Forey (1995) and Janvier (1996 a, b). Below we
discuss the implications for phylogeny where the
results of our analysis differ, and where new data
have provided a better understanding of character
evolution. Detailed paths of character changes are
shown optimised onto the most-parsimonious tree
after the deletion of pituriaspids (see above for
justification of this) ; Fig. 14 A shows ACCTRAN
optimisation while Fig. 14 B shows DELTRAN
optimisation. If there are equally parsimonious ways
of optimising a homoplastic character change (e.g. if
the alternatives mean that either the character has
been gained and independently lost, or that the
character is gained twice) then ACCTRAN favours
gain and loss while DELTRAN favours parallel
gains. A choice between these alternatives can only
be made by invoking ad hoc assumptions.
(b) Nervous and sensory systems
For over a century, hagfishes and lampreys have
been taken as proxies for the most primitive of
vertebrates and the condition of their organ systems
has been taken as the plesiomorphic condition
225
according to the scala naturae (Northcutt, 1981).
However, both hagfishes and lampreys are commonly thought to be wholly unrepresentative of the
ancestral vertebrate state (Northcutt, 1985), due to
their highly specialised modes of life (Conway
Morris, 1989b ; Northcutt, 1996 b) which are
reflected in an assumed derived morphology.
Northcutt (1981) and Wicht & Northcutt (1992)
have, therefore, adopted a cladistic approach to
resolving the condition of the hypothetical common
ancestor, or morphotype, at the respective nodes.
The topological relationship between hagfishes,
lampreys and jawed vertebrates that results from our
phylogenetic analysis concurs with many previous
studies and so reveals nothing more regarding the
evolution of the brain and sensory systems than
covered in the excellent reviews by Braun (1996),
Northcutt (1996 a), and Wicht (1996). However, a
number of subsequent studies have yielded data
pertinent to the early evolution of the brain and
sensory systems of vertebrates ; these were incorporated into our analysis and the implications of the
character changes which arise from our work are
discussed here.
Weigle & Northcutt (1998) have provided preliminary results of a restudy of the lamprey cerebellum which indicate that a cerebellum is not
present in lampreys. The optimisation used
(ACCTRAN ; Figs 14 A and 15) suggests that a true
cerebellum first evolved in conodonts. However, this
conclusion may be an artefact of optimising the
coding of this character (number 8) as a question
mark in Conodonta, Jamoytius, Euphanerops,
Anaspida, Eriptychius and Astraspis. Evidence for a
cerebellum occurs in heterostracans, galeaspids,
jawed vertebrates and osteostracans (and possibly
pituriaspids), and so a conservative estimate for the
origin of the cerebellum would be at the node
representing the common ancestor of heterostracans
and galeaspids (thus including Astraspis ; see Fig.
14 B, DELTRAN optimisation).
A sensory line system is first seen in Eptatretus, the
Pacific hagfish ; no other hagfish possesses a sensory
line system and the sensory hair cells of the
mechanoreceptors which comprise the sensory line
system are unpolarised and lack cupulae, both of
which are characteristic of true neuromasts. It is not
clear whether this condition is representative of the
plesiomorphic condition for vertebrates or results
from secondary reduction and eventual loss in other
hagfishes (Braun, 1996 ; Braun & Northcutt, 1997,
1998). Braun & Northcutt (1997, 1998) described
the presence of three groups of sensory grooves :
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
226
A
C
All zero
B
All zero
Conodonta
Conodonta
Tunicata
Cephalochordata
Cephalochordata
Tunicata
Myxinoidea
Myxinoidea
Petromyzontida
Petromyzontida
Anaspida
Osteostraci
Jamoytius
Galeaspida
Euphanerops
Pituriaspida
Loganellia
Eriptychius
jawed vertebrates
jawed vertebrates
Eriptychius
Loganellia
Pituriaspida
Euphanerops
Galeaspida
Jamoytius
Osteostraci
Anaspida
Astraspis
Astraspis
Arandaspida
Heterostraci
Heterostraci
Arandaspida
Tunicata
D
Tunicata
Conodonta
Cephalochordata
Cephalochordata
Conodonta
Myxinoidea
Myxinoidea
Petromyzontida
Petromyzontida
Anaspida
Galeaspida
Jamoytius
Pituriaspida
Euphanerops
Osteostraci
Loganellia
jawed vertebrates
jawed vertebrates
Eriptychius
Eriptychius
Loganellia
Pituriaspida
Jamoytius
Galeaspida
Euphanerops
Osteostraci
Anaspida
Astraspis
Astraspis
Arandaspida
Arandaspida
Heterostraci
Heterostraci
Fig. 12. (A–D) Constraint trees based on previous hypotheses of conodont affinity amongst the Chordata (see text for
discussion). (A, B) Dzik (1995) constraint trees ; (A) 42 trees, 192 steps, CIe 0.613, RI 0.694, RC 0.307 ; (B) 42 trees,
193 steps, CIe 0.609, 0.690, 0.422. (C) Kemp & Nicoll (1995b) constraint tree ; 42 trees, 190 steps, CIe 0.619, RI
0.650, RC 0.404. (D) Peterson (1994) and Pridmore et al. (1997) constraint tree ; 45 trees, 186 steps, CIe 0.632, RI
0.670, RC 0.425. Dotted lines represent taxa not considered in the original analysis.
Conodont affinity and chordate phylogeny
A
C
Tunicata
227
B
Tunicata
Cephalochordata
Cephalochordata
Conodonta
Myxinoidea
Myxinoidea
Conodonta
Petromyzontida
Petromyzontida
Galeaspida
Galeaspida
Pituriaspida
Pituriaspida
Osteostraci
Osteostraci
jawed vertebrates
jawed vertebrates
Eriptychius
Eriptychius
Loganellia
Loganellia
Jamoytius
Jamoytius
Euphanerops
Euphanerops
Anaspida
Anaspida
Astraspis
Astraspis
Arandaspida
Arandaspida
Heterostraci
Heterostraci
Tunicata
D
Tunicata
Cephalochordata
Cephalochordata
Myxinoidea
Myxinoidea
Conodonta
Petromyzontida
Petromyzontida
Jamoytius
Astraspis
Euphanerops
Arandaspida
Anaspida
Heterostraci
Eriptychius
Anaspida
Astraspis
Jamoytius
Arandaspida
Euphanerops
Heterostraci
Loganellia
Galeaspida
Eriptychius
Conodonta
jawed vertebrates
Loganellia
Osteostraci
jawed vertebrates
Pituriaspida
Osteostraci
Galeaspida
Pituriaspida
Fig. 13. (A–D) Constraint trees based on previous hypotheses of conodont affinity amongst the Chordata (see text for
discussion). (A) Krejsa et al. (1990 a, b) constraint tree ; 45 trees, 186 steps, CIe 0.632, RI 0.670, RC 0.425. (B)
Aldridge et al. (1986) constraint tree ; 45 trees, 182 steps, CIe 0.646, RI 0.689, RC 0.447. (C) Janvier (1996 b) constraint tree ; 3 trees, 182 steps, CIe 0.646, RI 0.689, RC 0.447. (D) Janvier (1995, hypothesis b) constraint tree ; 6
trees, 187 steps, CIe 0.629, RI 0.665, RC 0.420. Dotted lines represent taxa not considered in the original analysis.
1 1 5 5 5 5 5 4 4 2 2 2 2 1 1 1 1 1 1 7 6 5 2 1
0 0 6 4 3 2 1 6 3 7 6 5 0 8 7 6 4 1 0
3 1
0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 1 1 1 1 1 1 1
Cephalochordata
Fig. 14 a. For legend see opposite.
9 4 3 3 4
5 0 6 3
1
0
0
0
Tunicata
0 1 1 1 2
(a)
Myxinoidea
1 9 9 9 9 9 9 9 9 9 9 8 8 8 8 8 8 8 5 5 5 5 4 4 4 3 3 3 3 3 2 2 2 2 2 2 1 1 1 1 6
0 9 8 7 6 5 4 3 2 1 0 9 8 7 6 5 4 3 8 7 5 0 9 2 0 9 8 7 4 0 9 8 5 4 3 0 9 7 3 2
2
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 0 1 1 1 1 1 1 1 2 1 1 2 1 2 1 1 2
1 1
8 5
2 1
1 1 7 6 6 5 5 4 3 3 2 1 9 8 3
0 0 3 5 0 6 3 1 6 3 1 0
1 0
7 7 6 6 5
8 4 7 2 9
1 1 1 1 1
7 7
7 0
1 1
Petromyzontida
0 0 2 1 1 0 0 1 0 0 1 0 1 1 1
1 6 6 4 4 4 1
0 4 1 5 4 3 1
3
1 1 1 1 1 0 0
4 4 2
7 5 2
1 1 1
0 1
8 7 6 5 4 3 2
1 7 9 4 4 2 6
Jamoytius
8 7 6 6 4 4 4 3
2 1 4 3 9 8 7 0
8 7 7 7 4 3 3
0 8 7 6 5 5 1
1 2 0 1 0 1 1
6 6 4 2
8 7 3 7
6 6 3
8 7
Galeaspida
Osteostraci
8 7 7 6 4 3 1
2 3 1 9 8 2 5
1 0 0
Jawed
vertebrates
Eriptychius
6
6
1 0 0 0
1
0 1 0 0 0 0 1
7 6 5 4 2 1 1 1 4
0 9 2 0 0 7 6 4
1 2 0 1 3 0 0 1 1
Loganellia
1 1 1 1 2 1 0 0
7
3
1
Euphanerops
3
5
1
Anaspida
1 1 1 0 1 1 2
7 1
8 7
7
6
7 6 2
4 1 9
1
2 1 0
Arandaspida
Heterostraci
1 0 2
7 7 7
9 8 2
5 3 2
0 0 6
8 8 7 6 2
2 1 4 9 9
1 1 2 0 0
1 2 1
7 7 7 6 6 4 1
6 5 1 9 6 9 4
Astraspis
7 2 4
0 5
2 1 1
1 1 1 2 1 0 1
Conodonta
228
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Conodont affinity and chordate phylogeny
(b)
Tunicata
0 0 1
1 1
3 3
6 3
1 9 4
0 5 0
0
Cephalochordata
0 1 0 1 1 1 1 1 1 2 1 1 1 1 1
1 1 1 1 1 1 1 2 1 1 1 1
1 1 9 5 5 4 4 2 2 1 1 1 1 1 6
0 0 5 6 3 3 0 5 0 8 7 5 1 0
3 1
Myxinoidea
1 1 1 1 1 1 1 1
Petromyzontida
1 6 6 5 5 4 4 1
0 4 1 6 3 5 4 0
1
5 5 5 4 2 2 1 1 7 5 2 1
4 2 1 6 7 6 6 4
1 1
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1 2 1 1 2 1 1 2 1 1 2 2
7 7
7 0
1 9 9 9 9 9 9 9 9 9 8 8 8 8 8 8 8 5 5 5 5 4 4 3 3 3 3 3 2 2 2 2 2 2 1 1 1 1 1 6 4
0 9 8 7 6 4 3 2 1 0 9 8 7 6 5 4 3 8 7 5 0 9 2 9 8 7 4 0 9 8 5 4 3 0 9 8 7 3 2
2
Conodonta
2 2 1 1
Astraspis
2 1
1 1 1
7 6 2 4
0 9 5
1 1 2 0
7 7 6
5 1 6
1 2 1 1
8 8 7 2
2 1 4 9
7 7 7 7
9 8 6 2
2 1 0 0 2 1
7 6
3 5
Arandaspida
Heterostraci
6 5 4 3 2 1
9 0 9 0 6 4
1 1 1 1 1 1 1 1
1
7 7 6 6 4 2 8 3
8 4 7 2 3 1
2 1 0
7
6
7 4 2
4 7 9
0 1
7 6
8 1
Anaspida
1 1
3 1
5 7
Jamoytius
Euphanerops
1
1 1 1 1
4
5
7 7 6 4
7 3 9 7
Loganellia
1
1 1 2
1 1 2
4 3 2
4 2 6
7 7 6
1 0 9
1 1 1 1 1 2 1 0 1
Eriptychius
6
6
0 0 1 1 1 0 0 0 1 0 1 0 0 0 3 0 0 1 1 1 1
1 1 8 7 6 6 5 5 4 4 4 3 3 2 2 1 1 1 1 9 4
0 0 2 7 8 7 4 2 8 3 0 6 3 7 0 7 6 4 1
3 0
8 6 6 6 5 4 4 3 2
1 4 3 0 9 9 1 0 2
Jawed
vertebrates
1 1 1 1 0 1 0 0
1 2 1 1 1
8 7 7 3 3
0 8 6 5 1
8 7 6 6 6 4 4 3
2 1 9 8 7 8 5
1 0 1
7 3 1
3 2 5
Osteostraci
Galeaspida
Fig. 14. Character change trees ; each character change is denoted by a box below which appears the character number, and above
which appears the character state. Boxes and arrowheads represent the type of change : a solid black cell represents a synapomorphy,
a right-facing arrowhead represents a forward homoplasy, and a left-facing arrowhead represents a homoplasy reversal. (A) Under
ACCTRAN (accelerated transformation) optimisation. (B) Under DELTRAN (delayed transformation) optimisation. Diagrams
should be read in landscape.
229
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Tunicata
Cephalochordata
Myxinoidea
Petromyzontida
Conodonta
Astraspis
Heterostraci
Arandaspida
Anaspida
Jamoytius
Euphanerops
Loganellia
Eriptychius
Jawed vertebrates
Osteostraci
Galeaspida
230
26
25
24
23
22
21
20
19
18
17
16
15
14
13
12
11
10
9
8
7
6
5
4
3
2
1
a
GAIN: neural crest, brain, divided pituitary,
Adenohypophysis (simple), optic tectum, flattened
spinal chord, united d+v spinal nerve roots, single
median nasal opening, single nasohypophysial
opening (terminal), paired olfactory, single scc,
cranial lateral line grooves
b GAIN: segmented and compartmentalised
adenohypophysis, two types giant Mauthner cells,
synaptic ribbons in retinal receptors, dorsal
nasohypophysial opening, extrinsic eye musculature,
two scc, sensory-line neuromasts, electroreceptive cells,
sensory-lines on head and body
c GAIN: olfactory tract, cerebellum, pretrematic
d
e
f
g
h
branches of branchial nerves, flattened spinal
chord, vertical scc
GAIN: paired nasal openings
GAIN: externally open endolymphatic ducts
GAIN: terminal nasohypophysial opening
GAIN: sensory-line system enclosed in canals
GAIN: pineal present but uncovered, paired nasal
openings, 3 semicircular canals
LOSS: single nasohypophysial opening
f
h
d
g
e
c
a
b
Fig. 15. Nervous character distribution under ACCTRAN optimisation. Symbols represent different character states.
preoptic, dorsal postoptic, and ventral postoptic.
The preoptic grooves are innervated by a single pair
of ganglionated cranial nerves and the two postoptic
groove series are innervated by a pair of cranial
nerves which each possess two ganglia, possibly
resulting from the fusion of two pairs of ganglionated
nerves.
Many characteristics of the sensory line system of
lampreys are common to the lateral line system of
jawed vertebrates. The mechanoreceptors lack
cupulae and are composed of a polarised arrangement of sensory hair cells and occur as free
neuromasts arranged into a number of lines on both
the head and trunk (Johnston, 1905), many of which
have been homologised with counterparts in jawed
vertebrates (Northcutt 1985, 1989).
Sansom et al. (1997) have recently described the
presence of an asymmetrical pair of lateral line
grooves caudal to the pineal region of Astraspis,
possibly representing postpineal lines (they
questioned whether these structures are the same as
described by Stensio$ , 1964, p. 178). Heterostracans
possess a well-developed lateral line system enclosed
in canals which run through the middle layer of
Conodont affinity and chordate phylogeny
dermal skeleton ; possible homologies of gnathostome
lateral lines have been identified by Northcutt (1985 ;
1989) but it must be stressed that the pattern of
lateral line distribution is highly variable (Blieck,
1984). Sacabambaspis bears evidence of a lateral line
system where neuromasts were located in shallow
grooves in the dermal exoskeleton (Gagnier, 1993a),
possibly representing homologues of the supraorbital, infraorbital, mediodorsal (fragmented),
lateroventral longitudinal, and both dorsal and
ventral trunk lines, many of which are directly
comparable to the condition in heterostracans.
Smith (1957) described a number of shallow grooves
in the dermal skeleton of Pharyngolepis (an anaspid)
which he, and subsequently Northcutt (1989), were
able to identify as homologous with specific lines of
lampreys and gnathostomes ; evidence of a lateral
line system is not apparent in specimens of Jamoytius
or Euphanerops studied by us. The lateral line system
of thelodonts is generally poorly known although
Ma$ rss (1979) has described fully the condition for
Phlebolepis. Evidence from isolated scales indicates
that a lateral line system enclosed within specialised
canal scales occurred in Loganellia (P. C. J.
Donoghue, personal observations). The lateral line
system of osteostracans has been described and
discussed by Janvier (1974) and Northcutt (1985,
1989) although little is known of the distribution of
lines on the ventral surface of the head shield, or on
the trunk. The lateral line system of galeaspids is as
variable as in heterostracans, and the neuromasts
were situated within deep grooves which were
arranged in a scalloped pattern reminiscent of
anchipteraspids amongst heterostracans, but generally considered an autapomorphy of the
Galeaspida (e.g. Janvier, 1996a). In some polybranchiaspiforms, the lateral line system is enclosed
in canals which penetrate the dermal skeleton and
open at their extremity into pits which may represent
the sites of ampullary organs.
There is no clear pattern of evolution in the
condition of the lateral line system during this early
phase of vertebrate phylogeny. The mechanoreceptive hair cells of eptatretid hagfishes are located
in shallow grooves, as presumably were the neuromasts in lateral lines of Astraspis, arandaspids and
most galeaspids. In lampreys, neuromasts appear as
free organs arranged in lines (Kleerekoper, 1972),
and osteostracans are polymorphic, as the lateral
lines include both shallow grooves and sites of
individual free neuromasts (cf. Wangsjo$ , 1952).
Lateral lines arranged in canals have been attained
independently in heterostracans, thelodonts and
231
gnathostomes, and possibly also within other groups.
Thus, there is no evidence of a simple phylogenetic
pattern of free to canal-enclosed neuromasts. An
explanation may be afforded by consideration of
generalised lateral line development in gnathostomes
(Northcutt et al., 1994). If this model is applicable to
all lower vertebrates it is possible that the superficially random pattern of lateral-line evolution is
due solely to the effect of heterochronic patternproducing processes upon a compartmentalised
developmental sequence (e.g. Northcutt et al., 1994 ;
Braun & Northcutt, 1997 ; Northcutt, 1997). However, following Raff (1996), we recognise heterochrony only in its explanatory powers for recognising
and describing pattern ; heterochrony is not a
process.
The lack of definitive morphological criteria on
which the presence of electroreceptive capability can
be recognised in fossils leads to difficulty in interpreting the phylogeny of electroreception in vertebrates. Hagfishes possess no such capability (Braun,
1996) but lampreys are electroreceptive (Bodznick
& Northcutt, 1981 ; Bullock, Bodznick & Northcutt,
1983). Of the remaining jawless gnathostomes, only
the heterostracans, galeaspids and osteostracans
have been interpreted as having possessed electroreception. In heterostracans and osteostracans, it has
been suggested that the enigmatic pore canal system
is an extension of the lateral line system and that the
flask-shaped cavities within this system are the sites
of electroreceptors (Denison, 1951, 1964 ; Thomson,
1977 ; Northcutt & Gans, 1983 ; Northcutt, 1985).
More recently, however, evidence has been presented to cast doubt on the validity of this linkage.
The dermal skeleton of Palaeozoic lungfishes is
composed of a tissue combination known as cosmine
which is permeated by a pore canal system directly
comparable with the pore-canal systems of heterostracans and osteostracans. Bemis & Northcutt
(1992) demonstrated a comparable system of canals
in Recent lungfishes, which lack a mineralised
skeleton ; this canal-system is vascular and Bemis &
Northcutt (1992) suggested that the pore-canal
system in Palaeozoic lungfishes was similarly vascular, linked to the secretion and resorption of the
mineralised skeleton itself. Clearly, we can no longer
accept the presence of a pore-canal system as
undoubted evidence for electroreception ; more research is required.
Further evidence exists for electroreception in
osteostracans. Stensio$ (1927) suggested that the
cephalic sensory fields were the site of electroreceptors, although both Bohlin (1941) and Wangsjo$
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
Heterostraci
Arandaspida
Anaspida
Jamoytius
Euphanerops
Loganellia
Eriptychius
Jawed vertebrates
Galeaspida
Osteostraci
Tunicata
Cephalochordata
Myxinoidea
Petromyzontida
Conodonta
Astraspis
232
86
85
84
83
82
81
80
79
78
77
76
75
74
73
72
71
70
69
68
67
66
65
64
63
62
61
60
59
58
57
56
55
54
53
52
51
a
GAIN: neural crest, creatine phosphatase,
horny teeth, fin radials, visceral arches fused to
neurocranium
b GAIN: calcified dermal skeleton, polyodontida
LOSS: horny teeth
c GAIN: trunk dermal skeleton, lamellar aspidin,
diamond shaped-scales, dermal head covering
d GAIN: spongy aspidin, orthodentine, three-layered
exoskeleton, oak-leaf tubercles, oral plates
e
f
g
h
i
GAIN: cancellar layer, macromery, unpaired
headplates
GAIN: annular cartilage, rod-shaped scales,
LOSS: dermal head scales
GAIN: mesodentine, pharyngeal denticles,
scleroctic ossicles
GAIN: perichondral bone, calcified cartilage, three
layered exoskeleton,
j
GAIN: orthodentine, enamel
LOSS: visceral arches fused to neurocranium
k GAIN: oral plates, macromeric dermal head
scales, massive endoskeletal head shield
LOSS: pharyngeal denticles
e
g
j
k
i
f
d
h
c
b
a
Fig. 16. Hard tissue character distribution under ACCTRAN optimisation. Symbols represent different character
states.
Conodont affinity and chordate phylogeny
(1952) reinterpreted the fields as sites of mechanoreceptors. Northcutt (1985) also suggested that these
structures housed mechanoreceptors, representing
extensive evaginations of the membranous labyrinth.
Notwithstanding the function of the pore-canal
system or cephalic sensory fields of osteostracans,
Northcutt (1985) suggested that the presence of a
ramus lateralis communicans interconnecting the
ganglia of the anterior and posterior lateral line
nerves deduced to have been present in Procephalaspis
(Janvier, 1974) indicated that osteostracans were
electroreceptive, because this is a diagnostic feature
of electroreceptive species that possess trunk electroreceptors innervated by the lateral line nerve (Ronan
& Northcutt, 1987). Future research into the
phylogeny of electroreception, particularly amongst
the extinct groups of jawless gnathostomes might be
directed towards consideration of the relative arrangement of lateral line neuromasts and potential
evidence for the presence of electroreceptors ;
Northcutt, Bra$ ndle & Fritsch (1995) have demonstrated that both arise from common placodes in the
axolotl. Thus, evidence of a common association of
lateral lines and electroreceptors would provide
better evidence (e.g. Ørvig, 1971, for brachythoracid
arthrodires) than evidence for connection between
lateral line canals and putative electroreceptive
complexes (e.g. Denison, 1951).
(c) Skeleton
Although both hagfishes and lampreys are capable
of biomineralisation (Carlstro$ m, 1963) and lampreys
may be capable of calcifying their endoskeleton
(Bardack & Zangerl, 1971 ; Langille & Hall, 1993),
neither group expresses the ability to produce a
mineralised exoskeleton and both are assumed to be
primitively naked. The fossil record of hagfishes
extends back to the Upper Carboniferous (approximately 300 Ma ; Bardack, 1991), and the oldest fossil
lampreys are of Lower Carboniferous age (approximately 320 Ma ; Lund & Janvier, 1986). However,
because our analysis suggests that conodonts are
more derived than hagfishes and lampreys, and
because the fossil record of conodonts extends at least
as far back as the Late Cambrian (Aldridge &
Smith, 1993), our phylogeny indicates that the
hagfish and lamprey lineages are at least a further
220 and 200 million years older (respectively) than
their fossil record would suggest. This is not
surprising given that neither hagfishes nor lampreys
have been recovered from strata younger than Upper
233
Carboniferous (a subsequent gap of approximately
300 million years).
Our phylogenetic tree (Fig. 16 & see Fig. 17)
suggests that a mineralised skeleton evolved after the
origin of the hagfish and lamprey lineages, and is
first expressed in conodonts in the form of a
mineralised feeding apparatus composed from
odontodes of enamel and dentine. The next mostderived group of vertebrates are the pteraspidomorphs (sensu Gagnier, 1995, uniting Astraspis,
heterostracans and arandaspids), all of which possess
an extensively developed dermal exoskeleton composed predominantly from aspidin, with a subordinate component of orthodentine. This sequence
of character changes indicates that odontodes are the
primitive patterning unit of the vertebrate dermal
skeleton. As originally defined (Ørvig, 1967),
odontodes ‘ consist of dentine or dentinous tissue and
in most cases of superficial enameloid substance,
and...arise ontogenetically, each of them, in a single,
undivided dental papilla adjoined peripherally by
an epithelial dental organ of epidermis cells ’ (Ørvig,
1967 : p. 389). Reif (1982) later modified the
odontode concept to an isolated superficial structure
of the dermal skeleton which consists of a dentinous
tissue, a hypermineralised cap of enamel or
enameloid (which may or may not be present), and
a bony base (either cellular or acellular) which
functions as an attachment tissue ; the odontode
forms within a single, undivided dental papilla of
mesenchyme bounded at its outer surface by an
epithelial dental organ ; vascular supply through the
basal and\or neck canals ; attachment is enabled by
anchoring fibres which originate in the bony base, or
ankylosis to underlying bone. Thus far, no histologically investigated conodont exhibits evidence of
bone of attachment and it must be assumed that
primitively, odontodes were composed solely from
enamel and dentine ; bone of attachment must have
evolved after the divergence of conodonts. Evidence
for attachment tissues has been presented by Sansom
(1996), who described the presence of extinction
patterns in the dentine base of Pseudooneotodus
elements, which he interpreted as either backfilled
dentine tubules or attachment fibres ; comparison
with extinction patterns in the bone of attachment in
more derived vertebrates suggests that the latter
interpretation is most likely. The subsequent evolutionary history of bone and attachment tissues
depends critically upon the interpretation of aspidin
which comprises the basal layer of the heterostracan
exoskeleton.
Aspidin exists in many forms, some of which may
Vendian Cambrian
Ordovician
Dyfed
Bala
PRI
LLY
ASH
443
ARG
TRE
MER
CRF
543
EDI
VIS
TOU
354
m
l
LUD
417
Pituriaspida
Galeaspida
Osteostraci
Loganellia
Tertiary
Neogene
Tunicata
Jawed vertebrates
Conodonta
Petromyzontida
Myxinoidea
Cephalochordata
m
Eriptychius
u
206
Euphanerops
Triassic
u
Jamoytius
SPK
Heterostraci
Permian
LIA
Anaspida
Carboniferous
Mississippian
Pennsylvanian
UMI
Arandaspida
Devonian
Quaternary
Astraspis
Silurian
234
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
0
PLI
1.8
SCY
248
ZEC
ROT
GZE
290
KAS
MOS
BSK
WEN
CRD
LLO
LLN
490
STD
Fig. 17. Preferred phylogeny (grey) plotted against stratigraphic
ranges (black). Numbers are in millions of years before present.
Conodont affinity and chordate phylogeny
have different phylogenetic histories ; we have
attempted an initial first-fold division into lamellar
and spongy forms as part of this analysis. Aspidin is
traditionally interpreted as a form of acellular bone,
secondarily derived from cellular bone (Ørvig, 1951,
1965, 1989). However, Smith & Hall (1990) concurred with Denison’s (1967) interpretation of the
middle layer in Astraspis as trabecular dentine, but
also sided with Halstead Tarlo’s (1964) view that
early in vertebrate evolution aspidin and dentine
were hardly distinguishable. Denison (1967) also
interpreted the middle and basal layers of Eriptychius,
and the basal layer of Astraspis, as aspidin, and he
was able to distinguish dentine from aspidin on the
presence of odontoblast cell-processes incorporated
into the matrix of dentine (the middle layer) in
Astraspis ; Denison (1967) made no attempt to draw
homology between aspidin and any other vertebrate
hard tissue, although he rejected interpretations of
bone and dentine. Smith & Hall (1990 : p.302) cited
‘ the view that dentine is primitive and dentinerelated tissues (aspidin\cementum) formed in close
sequence, both in development, topographically and
in time, and in evolution ’. This view is based upon
the work of Palmer & Lumsden (1987) who, amongst
others (Ten Cate & Mills, 1972 ; Ten Cate, 1975 ;
Osborn, 1984 ; Osborn & Price, 1988), distinguished
skeletogenic and odontogenic components of the
vertebrate dermal skeleton, differentiating from the
dental papilla early in odontogenesis. It is not clear
how Smith & Hall (1990) interpreted the middle
layer in Astraspis or Eriptychius, but they returned to
Ørvig’s (1951, 1965, 1989) interpretation of the
basal layer of aspidin in various jawless vertebrate
groups as a homologue of bone of attachment, albeit
acellular, and an odontogenic derivative. Accepting
this interpretation of lamellar aspidin (alone), our
phylogenetic analysis suggests that acellular bone is
more primitive than cellular bone, concurring with
Maisey (1988) but contrary to Ørvig (1951, 1965,
1989), Smith & Hall (1990), Smith (1991) and
Sansom et al. (1992). In the absence of a phylogenetic
framework, Ørvig (1951, 1965, 1989) argued that
cellular bone was primitive for vertebrates ; in all
instances of acellular bone amongst jawed
vertebrates it could be demonstrated unequivocally
that cellular bone was primitive (Schaeffer, 1977 ;
Parenti, 1986). Smith & Hall (1990) and Smith
(1991) argued that cellular and acellular bone are of
equal antiquity because they are both found at the
same stratigraphic level. However, stratigraphy is no
basis for establishing polarity, and the oldest skeletal
remains to include cellular bone have since been
235
attributed to jawed vertebrates (Skiichthys ; Smith &
Sansom, 1997). Contrary to previous studies, our
analysis suggests that cellular bone evolved independently in jawed gnathostomes and osteostracans.
Maisey (1986) hypothesised that enamel tissues
were the first vertebrate hard tissues to arise, and the
distribution of characters in our analysis is superficially consistent with this proposal. However, the
distribution of enamel and enamel-like tissues
throughout the cladogram of relationships does not
appear to corroborate the hypothesis that enamel is
a synapomorphy of vertebrates (Smith, 1995).
Tissues which possess the structural and developmental characteristics of true (monotypic) enamel
are found in conodonts, Eriptychius and jawed
gnathostomes
(sarcopterygians
and
actinopterygians ; Smith, 1989, 1992). Enameloid has been
described from Astraspis (Denison, 1967 ; Reif, 1979 ;
Dzik, 1986 ; Smith et al., 1995) but its microstructure
cannot be compared to the enameloid of sharks and
actinopterygians (cf. Smith, Sansom & Smith, 1995).
Other records of enameloid in the dermal skeleton of
jawless vertebrates (e.g. osteostracans Stensio$ , 1927 ;
Belles-Isles, 1989 ; galeaspids Janvier, 1990 ; Zhu &
Janvier, 1998) mistake the distinction between
hypermineralised dentine and true enameloid ; there
is no evidence for a basal lamina between the
putative enameloid and the underlying ectomesenchymally derived tissue.
Conodont elements also incorporate (usually) an
atubular dentine (this is not evident from the distribution of characters on Fig. 14 A because atubular
dentine is not found in any of the other vertebrates included in the analysis, and so could not help resolve
relationships). The systematic position of conodonts
and the distribution of dentine types over the
cladogram would appear to indicate that atubular
dentine is more primitive than tubular dentines.
However, Huysseune & Sire (1998) have suggested
that atubular dentines result from spatially confined
development. Considering the small size of conodont
elements, and the presence of tubular dentines in
only the largest of elements (mesodentine and,
possibly, orthodentine ; Sansom et al., 1994 b), our
evidence would support this conclusion. Nevertheless, the presence of dentine in conodont elements
indicates that dentine is at least as primitive as
enamel, and the presence of a dentine in the absence
of bone or a bone-like tissue indicates that dentine
appeared before bone. Progressing from the root of
the cladogram, orthodentine is first found in
pteraspidomorphs. Mesodentine unites Loganellia
236
with its sister-group, although Eriptychius plus jawed
vertebrates are distinguished by the possession of
orthodentine. The random pattern of dentine types
apparent from the topology of relationships in our
most-parsimonious tree suggests that the structural
divisions between dentine types may be artificial,
resulting from epigenetic factors which are incongruent with phylogeny.
The random distribution of dentine structural
types brings into focus the random distribution of
hard tissues in general ; this is not a new observation.
The random distribution of histological characters
has generally been accounted for by the plasticity of
the odontode (Schaeffer, 1977). Conversely,
Halstead (1982) saw no such pattern, placing all his
faith in the a priori assumed importance of histological (plus other) characters to reconstruct
phylogeny. Schaeffer (1977) and Smith & Hall
(1990,1993) established the now prevalent view that
the odontode is ‘ a single, modifiable, morphogenetic
system ’ such that any of the component tissues
(enamel, enameloid, dentine, bone, cartilage) could
be absent or present in combination with any other,
and Smith & Hall (1993 : p. 395) have suggested
that the random pattern may result from the effect of
heterochrony upon the odontode differentiation program. The role of heterochronic processes in the
development of enamel versus enameloid was established by Shellis & Miles (1974 ; but see also Smith,
1989, 1992, 1995). Evidence for loss and subsequent
reappearance of other odontogenic tissues is based
upon heterotypic tissue recombinations in which a
taxon which is presumed, through lack of expression,
to have lost the ability to produce a tissue during
phylogeny can be demonstrated experimentally to
have retained the potential. The obvious example is
the experiment conducted by Kollar & Fisher (1980)
in which avian mandibular epithelium was demonstrated to retain a capability for ameloblast differentiation and enamel synthesis, when recombined with
murine dental papilla ectomesenchyme (see Kollar,
1998, for a discussion on the state of the debate over
this experiment). However, understanding of the
possible mechanisms is based on a highly generalised
summary of experiments based on very divergent
taxa. Moss (1964) argued that ‘ the earliest ossified
vertebrates possessed the intrinsic capacity to produce the entire spectrum of vertebrate skeletal
tissues’ ; in effect that the developmental program of
odonto\skeletogenesis (now perceived to be two
exoskeletal subsystems which arise from a common
cell population ; Palmer & Lumsden, 1987 ; Hall,
1992 ; Smith & Hall, 1990, 1993) had not been
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
canalised and thus was open to a great deal of
experimentation through natural selection. This
equates well with the view of phylogenetic reduction
in histological diversity in, for example, conodonts,
heterostracans (Halstead, 1987) and vertebrates in
general (Sansom et al., 1994b ; Smith et al., 1996).
Obviously, it is not possible to test these hypotheses
directly because the animals in which the developmental system was established have long been
extinct and there are no closely related living models.
Nevertheless, the skeleton is the one organ system in
which a record of development is potentially preserved in the fossil record and careful examination of
the pattern of development of the exoskeleton
topologically and across different taxonomic levels,
may yet provide a test of such hypotheses. Furthermore, a shift in focus from the study of
odontogenesis from traditional model animals with
their inherent problems (Bolker, 1995) to taxa which
are phylogenetically more critical to this problem
(e.g. Polypterus ; to some extent this shift in focus
has begun – see Huysseune & Sire, 1998) might
provide the basis for elegant experiments to test the
coherence of the odontode model.
V. CONODONT AFFINITY
‘ It is suggested that the present state of knowledge does not
justify a final conclusion as to the affinities of the conodonts,
although they appear to represent an extinct group of either
worm-like creatures or primitive vertebrates ’ (Rhodes,
1954 : p. 450).
Although Rhodes (1954) vacillated about the
affinities of conodonts it is clear that he favoured a
relationship to the annelids. He expressed reservations about an affinity with vertebrates, which
appeared ‘ to rest upon the answer to the question
‘‘ Must the chemical composition of the conodonts
(calcium phosphate) be interpreted as evidence of a
vertebrate origin, or is it possible for worms to secrete
such a substance internally ?’’ ’ (Rhodes, 1954 : pp.
448–449). We now know that annelids are capable of
biomineralisation using calcium phosphate (e.g.
Lowenstam, 1981), but no one any longer supports
the hypothesis that conodonts are annelids.
Our phylogenetic analysis provides unequivocal
support for the hypothesis that conodonts are
vertebrates, and not only in the widely used sense of
vertebrates l craniates (e.g. Donoghue et al., 1998),
but also in the sense used by Janvier (1981, 1993,
1996 a, b). Furthermore, our analysis suggests that
Conodont affinity and chordate phylogeny
A
crown-group
total-group
TØ
stem-group
crown-group
Gnathostomata
B
total-group
Gnathostomata
stem-group
Gnathostomata
Fig. 18. Stem, crown and total group classification. (A)
Theory. (B) Practice.
conodonts are more derived than lampreys, and in
accordance with Jefferies ’ (1979) criteria for recognising stem and crown groups (Fig. 18 A, B),
conodonts are stem-Gnathostomata. Although
crown and total groups can be given separate names
(de Queiroz & Gauthier, 1992), this approach results
in an unnecessarily expanded classification scheme
and in one of the groups (stem-group) being
paraphyletic (unless that group is represented by one
species only, in which case the need for a higher
group name is unnecessary). Generally, only the
total group is recognised by formal Linnean rank
(Patterson, 1993 ; Smith, 1994). Thus, conodonts
belong to the Gnathostomata ; they are gnathostomes, albeit without jaws (Fig. 18 B).
The results of this analysis indicate that conodonts
lie in a position between the living jawless vertebrates, which lack a mineralised exoskeleton, and
the extinct groups of jawless vertebrates which
possessed a mineralised exoskeleton in the form of a
dermal armour. Recodings in the experimental
section of this paper demonstrate that the affinity of
conodonts does not rest upon histological characters.
237
Homology of conodont and vertebrate hard tissues
would appear to be supported by congruence.
Within the constraint that conodonts are vertebrates
the conclusion that conodont hard tissues are an
independent experiment, acquired in parallel with
the common ancestor of the Pteraspidomorpha and
all other vertebrates, appears unlikely. Thus, hypotheses of conodont affinity which argue that
conodont hard tissues are autapomorphic, e.g. Dzik
(1995), Kemp & Nicoll (1995 a) and Pridmore et al.
(1997 ; see also Peterson 1994), are (respectively) 13,
10 and six steps longer than the optimal phylogenetic
position for conodonts, based upon our data set.
Nevertheless, the acquisition of a mineralised skeleton concomitant with a highly specialised feeding
apparatus does appear to occur very suddenly.
However, if the ancestors of conodonts (in our sense)
lie amongst the paraconodonts, there may be
evidence that this group of characters did not appear
all at once ; paraconodonts may prove to be sclerites
composed solely from dentine (cf. Bengtson, 1976)
and the origin of (eu)conodonts may be signalled by
the origin of enamel which, according to our
preferred phylogeny must have appeared more than
once (Fig. 14). However, patterning in the growth of
paraconodont elements appears to suggest that they
too grew appositionally, although an epithelial
component is not present, or at least not preserved.
Providing the homology between paraconodont
elements and euconodont basal bodies is correct, the
pattern of growth requires an epithelial contribution
to have been present, a possible candidate being
keratin, which has a very low preservation potential
(Davis & Briggs, 1995 ; Davis, in press).
Following Schmidt & Mu$ ller (1964) and Priddle
(1974), Krejsa et al. (1990 a, b) have argued that
hagfish toothlets and conodont elements are homologous, although their hypothesis has here been
rejected because the primary observations are clearly
inconsistent with the pattern of morphogenesis
exhibited by conodont elements (Szaniawski &
Bengtson, 1993 ; Smith et al., 1996 ; Donoghue,
1998). However, recent reappraisal of reports on the
presence of enamel-like antigens in the pokal cell
cone of hagfish toothlets (Slavkin et al., 1983 ; see
Slavkin & Dieckwisch, 1996, 1997), together with
analysis of toothlet microstructure (Dieckwisch &
Vahadi, 1997), require that we look at this hypothesis anew. Slavkin & Dieckwisch (1996, 1997)
have demonstrated the presence of amelogenins not
only in the enigmatic pokal cells, but also within the
keratin itself, with particular concentrations in the
near-surface layers of the toothlets (but see Girondot,
238
Delgado & Laurin, 1998). Dieckwisch & Vahadi
(1997) also determined that the toothlets have a high
calcium to phosphate ratio and even found evidence
of keratin mineralisation. Krejsa et al. (1990 b)
speculated that, were keratin heavily mineralised, it
would resemble the lamellar crown tissue of conodont elements (although see Slavkin & Dieckwisch,
1996). However, we now know of many instances of
mineralised keratin (T. G. H. Dieckwisch, personal
communication, 1998) and these are not comparable
histologically to conodont hard tissues. Nevertheless,
the possibility that hagfishes (and possibly lampreys)
express the plesiomorphic condition for the vertebrate dermal skeleton must be considered more
seriously.
Smith & Hall (1990) argued that conodont
elements and hagfish toothlets were independent
experiments with skeletal biomineralisation and
Young, Karatajute-Talimaa & Smith (1996) considered the conodont skeleton to be an independent
specialisation which diverged from other vertebrates
soon after the establishment of the vertebrate
skeleton. Indeed, Smith & Coates (1998) have
argued that the conodont skeleton may be an entirely
distinct experiment in oral skeletal structures. However, available evidence suggests that the conodont
skeleton is the earliest expression of skeletal biomineralisation amongst vertebrates, and that an
oropharyngeal skeleton\dentition is plesiomorphic
for the clade. Whether conodont elements are
homologous to true teeth is a moot point. They
clearly do not occur topologically within a jaw, but
they do exhibit evidence of replacement (Donoghue,
1998 ; Donoghue & Purnell, 1999 a) ; they also grew
in a manner directly comparable to teeth (Schmidt
& Mu$ ller, 1964 ; Mu$ ller & Nogami, 1971 ; Sansom,
1996 ; Donoghue, 1998), functioned like teeth
(Purnell, 1995 ; Donoghue & Purnell, 1999 b), and
even look like teeth (Pander, 1856 ; Jeppsson, 1979).
VI. DIRECTIONS FOR FUTURE RESEARCH
(1) General
Recent years have seen a dramatic increase in our
understanding of many aspects of conodont palaeobiology, leading to the results presented in this
paper. However, the apparent magnitude of these
advances simply reflects how little was previously
known, and there is still much to do. Sweet (1988 : p.
189) estimated the number of named conodont
species at ‘ nearly 5000 ’, although he considered only
1446 species and 246 genera to be ‘ reasonably
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
distinct in a multielement context ’. These values
should be taken as a highly conservative estimate
(Sweet, 1988 : p. 131) ; even so, conodonts comprise
almost 65 % of all known jawless vertebrates, and
2.8 % of total vertebrate diversity, living and extinct
(by comparison with figures in Nelson, 1994).
Despite this, and despite the importance of conodonts in interpretations of early vertebrate evolution,
we remain ignorant of all but the most fundamental
aspects of conodont palaeobiology and evolution.
Below, we outline some of the major unanswered
questions and outstanding problems.
(2) The origin of the Conodonta
Debate over the affinity of the group has reached a
state of maturity and will progress further only with
discovery of unexpected new anatomical data.
However, as we signalled with a caveat over the
monophyly of the Conodonta at the beginning of this
paper, we remain unaware of the direct ancestry of
the group. Little is known regarding the apparatus
architecture of the early Teridontus and Proconodontus
lineages ; the overall similarity in growth patterns
and histology shown by these two putative clades
suggests that they are closely related, but the
question remains, how closely ? Resolution of this is
most likely to rest with the unravelling of the
relationships between these lineages and the paraconodonts (following Bengtson, 1976). However, the
paucity of diagnostic features in these groups means
that determination of these relationships will be very
difficult. The paraphyletic paraconodonts are distinguished from euconodonts by the absence of a
character, i.e. a crown composed from a discrete
tissue type. On current knowledge, the only potential
synapomorphy of para- and (primitive) euconodonts
is the possession of phosphatic cone-shaped sclerites
which grow by episodic secretion of successive layers
that only partially encapsulate preceding layers.
Sclerites from many other groups also exhibit a
grade of organisation which parallels this, and so we
need to assess whether there is any evidence that
para- and euconodonts should be linked at all.
Cambrian strata yield a wide variety of microscopic phosphatic sclerites, several of which possess
histological attributes that might suggest comparison
with microvertebrate remains. For example, sclerites
referred to the genera Hadimopanella and Milaculum
have in the past been allied to the jawless vertebrates
on the basis of tissues that resemble enamel and
dentine (see e.g. Dzik, 1986). However, Hinz et al.
(1990) and Mu$ ller & Hinz-Schallreuter (1993) have
Conodont affinity and chordate phylogeny
demonstrated unequivocally that these microremains belong to a group of hitherto poorly known
Palaeozoic annelids, the Palaeoscolecida. This discovery highlights the problems of using histological
data alone to determine relationships, without the
benefit of a broader anatomical context.
One way to demonstrate a link between paraconodont and euconodont elements would be to
document a series of intermediate forms. This
approach was adopted by Szaniawski & Bengtson
(1993), who described specimens that resemble
paraconodonts in early ontogeny but appear to
acquire a crown in late ontogeny. Histogenetic
investigation of such specimens should show that
mature sclerites display no correlation between
incremental layers in the base and crown in the
portion of the growth record representing early
ontogeny ; unfortunately, this is not clearly demonstrated in any of their material.
More recently, Mu$ ller & Hinz-Schallreuter
(1998) have described the histology of Westergaardodina sp., clearly a paraconodont in its grade of
histological organisation, which displays a calcospheritic microstructure directly comparable with
the basal body of the euconodont Cordylodus (e.g.
Mu$ ller & Nogami, 1971 ; Sansom et al., 1992 ;
Aldridge & Donoghue, 1998). An even more
persuasive link is evident in the histology of
Serratocambria minuta Mu$ ller & Hinz, also described
by Mu$ ller & Hinz-Schallreuter (1998), in which the
pattern of growth is comparable with the basal body
of much younger, highly derived euconodont taxa
(e.g. Carniodus in Donoghue, 1998).
It remains an open question whether acquisition
of a phosphatic crown unites the Teridontus and
Proconodontus lineages, or whether the crown evolved
more than once. This can only be resolved by
determining relationships between the taxa of paraconodonts and primitive euconodonts and thereby
testing the traditional grade-based groupings.
(3) Euconodont phylogeny
The adoption of a wholly artificial form-taxonomy
for elements during the first century of conodont
research meant that it was impossible to construct a
meaningful scheme of high level classification. With
the rise of multielement taxonomy (e. g. Huckreide,
1958 ; Walliser, 1964 ; Bergstro$ m & Sweet, 1966 ;
Webers, 1966), however, the basis was provided for
the development of a homology-based scheme
(Sweet & Scho$ nlaub, 1975 ; Sweet, 1981, 1988 ;
Purnell et al., 2000), although there has been little
239
progress towards a truly hierarchical suprageneric
system. The most recent classifications (Sweet, 1988 ;
Dzik, 1991) are dominated by groupings that are
unashamedly para- and polyphyletic, as recognised
by Aldridge & Smith (1993), who nevertheless
adopted a modified version of the Sweet (1988)
scheme. It is now appropriate to undertake more
rigorous analyses of relationships within the conodonts to produce a classification based on monophyletic groups ; the implementation of cladistic
methodology should be aided by the fact that current
conodont taxonomy is largely based on topological
homology. There is some urgency here, because until
conodont phylogeny has been unravelled, we cannot
advance our understanding of the evolution of
element histology, growth and function.
(4) Histology
The vertebrate skeleton is the system of choice for
studying organ development in biological and
biomedical research (Hall, 1992). Its evolutionary
history is also more easily understood than that of
any other organ system, because it is mineralised and
therefore readily fossilised. The results of our
phylogenetic analysis are congruent with the hypothesis that the vertebrate dermal skeletal system
was established in the common ancestor of conodonts
and more-derived vertebrates after separation of the
lamprey lineage. Conodonts are therefore an ideal
model group in which to study the evolution of the
skeletal developmental system : the conodont clade
persisted for some 300 million years, showing low
disparity and high diversity, and the elements exhibit
a very wide range of hard tissue and morphogenetic
diversity.
The existing histological database shows that the
odontogenic system in conodonts underwent considerable change during the phylogeny of the group
(Smith et al., 1996 ; Donoghue, 1998). However, only
a small percentage of conodont taxa have been
investigated histologically. Of the seven orders of
conodonts proposed by Sweet (1988), only representatives of the Ozarkodinida, the most derived
group, have been studied in any detail (Donoghue,
1998), and the results are probably not representative of the conodont clade as a whole. Published
histological data from the remaining six orders
(Proconodontida,
Belodellida,
Protopanderodontida, Panderodontida, Prioniodontida, Prioniodinida) are largely restricted to abstract accounts
(summarised in Donoghue, 1998). Limited research
on the Panderodontida, an equally derived but
240
divergent group of conodonts, has revealed an
entirely different mode of growth from that shown
by ozarkodinids (Barnes, Sass & Poplawski, 1973),
and preliminary studies of the Prioniodontida
(Donoghue & Chauffe, 1999) have demonstrated
the presence of a unique suite of hard tissue types.
Most critically, histological data on primitive conodonts are extremely limited.
(5) Microevolution
As has been pointed out in other reviews of
conodonts, the elements hold clear potential for
microevolutionary studies. Although the useable
record of conodonts is limited exclusively to their
teeth, these show clear sequential changes and often
occur in great numbers. There have been several
morphometric studies of conodont elements over the
years (e.g. Rhodes, Williams & Robinson, 1973 ;
Barnett, 1971 ; Croll, Aldridge & Harvey, 1982 ;
Croll & Aldridge, 1982 ; Murphy & Matti, 1982 ;
Murphy & Cebecioglu, 1986, 1987 ; Klapper &
Foster, 1986, 1993), but to date there have been few
serious attempts to use the conodont record as a
testing ground for hypotheses of evolutionary
patterns and processes.
(6) Conodont element function
The documentation of microwear features on the
surfaces of a variety of conodont elements (Purnell,
1995) has provided clear evidence that they performed a tooth function. Investigation of the
functional morphology of molarised elements of the
Pennsylvanian conodont Idiognathodus (Donoghue &
Purnell, 1999 b) has also shown that these occluded
so precisely that no room would have been available
for any intervening soft tissue cover. There is a need
to reconcile the appositional growth of these elements
with their occlusive function, and this may be
explained by evidence of periodic soft tissue cover
(Donoghue & Purnell, 1999 a).
Although the functional morphology of some
elements of a few taxa has now been interpreted in
some detail, very little is still known regarding
element and apparatus function in general. Coniform taxa are particularly poorly understood, the
only current direct evidence arising from surface
scratches on an element of Drepanoistodus figured by
Purnell (1995). In the more complex apparatuses,
studies have been largely directed at the posteriormost P elements, with limited data also available on
"
the function of the P elements. Our knowledge of
#
the functions of M and S elements currently amounts
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
to little more than informed conjecture. Detailed
investigations are now required of diverse, wellpreserved taxa, set in a clear phylogenetic context.
In this way, it should become possible to establish
the functional adaptations and constraints driving
the morphological evolution of the euconodont
clade(s).
VII. REVISED CLASSIFICATION
In our Linnean rank-free classification below we use
a total group concept (see Fig. 18) in which taxa
forming a stem-lineage series leading to a crown
group are classified as members of the total group.
This is the most unambiguous way of specifying
phylogenetic relationships. We also use the
sequencing convention of Nelson (1972), the plesion
rank as introduced by Patterson & Rosen (1977) and
the sedis mutabilis suffix introduced by Wiley (1979).
Craniata Linnaeus, 1758
Myxiniformes Berg, 1940
Vertebrata Linnaeus, 1758
Petromyzontiformes Berg, 1940
Gnathostomata Cope, 1889
plesion Conodonta Eichenberg, 1930
plesion Pteraspidomorphi Goodrich, 1909
Astraspis
Heterostraci Lankester, 1868
Arandaspidiformes Ritchie & GilbertTomlinson, 1977
plesion unnamed group A
plesion Anaspida Traquair, 1899
Jamoytius
Euphanerops
plesion Loganellia
Unnamed group B
Eriptychius
Jawed vertebrates
plesion unnamed group C
Osteostraci Lankester, 1868 sedis mutabilis
Pituriaspida Young, 1991 sedis mutabilis
Galeaspida Halstead, 1982 sedis mutabilis
VIII. CONCLUSIONS
(1) The presence of myomeres and a notochord in
body fossils of euconodonts justifies interpretation of
the group in the context of a chordate bauplan.
(2) The significance of conodonts to our understanding of chordate evolution cannot be assessed by
placing the group within an existing hypothesis of
Conodont affinity and chordate phylogeny
phylogenetic relationships, based upon a priori
determined synapomorphy distribution.
(3) Cladistic analyses show that conodonts are
vertebrates and that they are more derived than
either hagfishes or lampreys because they possess a
calcified dermal skeleton ; this phylogenetic position
does not rely on the nature of the mineralised tissues.
(4) The Conodonta are stem-group Gnathostomata ; paraconodonts and euconodonts are the
most primitive members of the total-group Gnathostomata.
(5) The mineralised vertebrate skeleton first
appeared as odontodes of dentine or dentine plus
enamel in the paraconodont\euconodont feeding
apparatus. The later appearance of bone was linked
to the development of an external dermal skeleton ;
bone appears to have been initially acellular.
(6) Atubular dentine is more primitive than
tubular dentine.
(7) There was no simple, single evolutionary
transition from free neuromasts to canal-enclosed
neuromasts in the early phase of vertebrate history.
(8) The most primitive vertebrates lacked biomineralised skeletons ; myxinoids and petromyzontids were in existence at least by the early
Cambrian.
IX. ACKNOWLEDGEMENTS
We thank Stefan Bengtson (NRM, Stockholm), Glenn
Northcutt (Scripps & UCSD), Mark Purnell (Leicester),
Moya Smith (KCL & Guys) and Paul Smith
(Birmingham) for comments, and Philippe Janvier
(MNHN, Paris) and an anonymous other for useful
reviews of the manuscript. We gratefully acknowledge V.
Viira (Tallinn) and P. H. von Bitter (ROM, Toronto) for
providing some of the specimens from which histological
sections were prepared. The following have either
supplied data or images, or discussed topics from which
ideas expressed in this manuscript have benefited : C. B.
Braun (Parmly Inst., Chicago), N. D. L. Clarke (Hunterian, Glasgow), J. Dzik (PAN, Warszawa), D. Goujet
(MNHN, Paris), J. K. Ingham (Hunterian Museum,
Glasgow), P. Janvier (MNHN, Paris), R. P. S. Jefferies
(NHM, London), T. C. Lacalli (Saskatchewan), R. G.
Northcutt (Scripps & UCSD), M. A. Purnell (Leicester),
David J. Siveter (Leicester), M. M. Smith (KCL &
Guys), M. P. Smith (Birmingham), I. J. Sansom
(Birmingham), M. J. Telford (NHM, London) and C.
Weigle (THH, Hannover). A. Milodowski (BGS,
Keyworth) collaborated in SEM studies of conodont
extrinsic eye musculature. We are particularly grateful to
K. A. Freedman (Leicester) for sharing with us the details
of her latest investigation of the anatomy of Jamoytius
kerwoodi. Figures 3 a, c, d are reproduced herein with the
241
permission of the Lethaia Foundation ; Figures 4 b, d, e
are reproduced with the permission of Macmillan
Magazines Ltd ; Figures 5 d, g, h are reproduced with the
permission of the Geological Society of America ; Figures
5 k, l are reproduced with the permission of the Paleontological Society. Donoghue was funded by an 1851
Research Fellowship from The Royal Commission for the
Exhibition of 1851 and a NERC post-doctoral research
fellowship (GT5\99\ES\2).
X. REFERENCES
A, R. J. (1987). Conodont palaeobiology : a historical
review. In Palaeobiology of Conodonts (ed. R. J. Aldridge), pp.
11–34. Ellis Horwood, Chichester.
A, R. J. & B, D. E. G. (1986). Conodonts. In
Problematic Fossil Taxa. Oxford Monographs on Geology and
Geophysics No. 5 (eds. A. Hoffman and M. H. Nitecki), pp.
227–239. Oxford University Press, New York.
A, R. J., B, D. E. G., C, E. N. K. &
S, M. P. (1986). The affinities of conodonts – new
evidence from the Carboniferous of Edinburgh, Scotland.
Lethaia 19, 279–291.
A, R. J., B, D. E. G., S, M. P., C,
E. N. K. & C, N. D. L. (1993). The anatomy of conodonts. Philosophical Transactions of the Royal Society of London,
Series B 340, 405–421.
A, R. J. & D, P. C. J. (1998). Conodonts : a
sister group to hagfish ? In The Biology of Hagfishes (eds. J. M.
Jørgensen, J. P. Lomholt, R. E. Weber and H. Malte), pp.
15–31. Chapman & Hall, London.
A, R. J. & P, M. A. (1996). The conodont
controversies. Trends in Ecology and Evolution 11, 463–468.
A, R. J., P, M. A., G, S. E. & T,
J. N. (1995). The apparatus architecture and function of
Promissum pulchrum Kova! cs-Endro$ dy (Conodonta, Upper
Ordovician), and the prioniodontid plan. Philosophical Transactions of the Royal Society of London, Series B 347, 275–291.
A, R. J. & S, M. P. (1993). Conodonta. In The
Fossil Record 2 (ed. M. J. Benton), pp. 563–572. Chapman and
Hall, London.
A, R. J., S, M. P., N, R. D. & B,
D. E. G. (1987). The architecture and function of Carboniferous polygnathacean conodont apparatuses. In Palaeobiology
of Conodonts (ed. R. J. Aldridge), pp. 63–76. Ellis Horwood,
Chichester.
A, R. J. & T, J. N. (1993). Conodonts with
preserved soft tissue from a new Upper Ordovician KonservatLagerstaW tte. Journal of Micropalaeontology 12, 113–117.
A, D. (1988). Strukturen, apparate und phylogenie
primitiver conodonten. Palaeontographica Abt. A 200, 105–152.
A, M. & J, P. (1991). The anaspid-like
craniates of the Escuminac Formation (Upper Devonian)
from Miguasha (Que! bec, Canada), with remarks on anaspidpetromyzontid relationships. In Early Vertebrates and Related
Problems of Evolutionary Biology (eds. M. M. Chang, Y. H. Liu
and G. R. Zhang), pp. 19–40. Science Press, Beijing.
B, E. (1981). Primary sensory cells in the skin of
amphioxus (Branchiostoma lanceolatum (P)). Acta Zoologica
(Stockholm) 62, 147–157.
242
B, C. V. H. & B-F, M. (1997). The origins of
the neural crest. Part II : an evolutionary perspective.
Mechanisms of Development 69, 13–29.
B, D. (1991). First fossil hagfish (Myxinoidea) : a record
from the Pennsylvanian of Illinois. Science 254, 701–703.
B, D. (1998). Relationship of living and fossil hagfishes.
In The Biology of Hagfishes (eds. J. M. Jørgensen, J. P.
Lomholt, R. E. Weber and H. Malte), pp. 3–14. Chapman &
Hall, London.
B, D. & Z, R. (1968). First fossil lamprey : a
record from the Pennsylvanian of Illinois. Science 162,
1265–1267.
B, D. & Z, R. (1971). Lampreys in the fossil
record. In The Biology of Lampreys (eds. M. W. Hardisty and
I. C. Potter), pp. 67–84. Academic Press.
B, C. R., S, D. B. & P, M. L. S. (1973).
Conodont ultrastructure : the Family Panderodontidae. Royal
Ontario Museum, Life Sciences Contributions 90, 1–36.
B, S. G. (1971). Biometric determination of the evolution
of Spathognathodus remscheidensis : a method for precise intrabasinal time correlations in the northern Appalachians.
Journal of Paleontology 45, 274–300.
B, I. S., M, T. A. & S, L. P. (1982).
New evidence for the vertebrate nature of the conodontophorids. Paleontological Journal 1982(1), 82–90.
B-I, M. (1989). Mise en e! vidence di l’endosquelette
postcra# nien chez un Oste! ostrace! , Alaspis multituberculata Ørvig,
du De! vonien supe! rieur de Miguasha (Quebec). Compte Rendu
AcadeT mie des Sciences de Paris, SeT rie II 308, 1497–1501.
B, W. E. & N, R. G. (1992). Skin and blood
vessels of the snout of the Australian lungfish, Neoceratodus
forsteri, and their significance for interpreting the cosmine of
Devonian lungfishes. Acta Zoologica (Stockholm) 73, 115–139.
B, S. (1976). The structure of some Middle Cambrian
conodonts, and the early evolution of conodont structure and
function. Lethaia 9, 185–206.
B, S. (1983 a). A functional model for the conodont
apparatus. Lethaia 16, 38.
B, S. (1983 b). The early history of the conodonta.
Fossils and Strata 15, 5–19.
B, L. S. (1940). Classification of fishes, both recent and fossil.
Travaux de l’Institute Zoologique de l’AcadeT mie des Sciences de
l’URSS 5, 1–517. [in Russian with English translation 1947].
B$ , S. M. & S, W. C. (1966). Conodonts from the
Lexington Limestone (Middle Ordovician) of Kentucky and
its lateral equivalents in Ohio and Indiana. Bulletins of
American Paleontology 50, 271–441.
B, A. (1984). Les He! te! rostrace! s pte! raspidiformes, agnathes
du Silurien-De! vonien du continent Nord-Atlantique et des
Blocs Avoisnants : re! vision syste! matique, phyloge! nie, biostratigraphie, bioge! ographie. Cahiers de Pale! ontologie,
Centre national de la Recherche scientifique, Paris.
B, D. & N, R. G. (1981). Electroreception in
lampreys : evidence that the earliest vertebrates were electroreceptive. Science 212, 465–467.
B, B. (1941). The dorsal and lateral cephalic fields in the
Osteostraci. Zoologiska Bidrag Frab n Uppsala 20, 543–554.
B, J. A. & R, R. A. (1995). Model systems in
developmental biology. BioEssays 17, 451–455.
B, T., B, P. W. & T, M. C. (1993).
Substancep- and cholecystokinin-like immunoreactivity during post-metamorphic development of the central nervous
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
system in the ascidian Ciona intestinalis. Cell and Tissue Research
272, 545–557.
B, T., B, P. W. & T, M. C. (1997).
Investigation of the contribution from peripheral GnRH-like
immunoreactive ‘ neuroblasts ’ to the regenerating central
nervous system in the protochordate Ciona intestinalis. Proceedings of the Royal Society of London, Series B 264, 1117–1123.
B, T., H, S., T, M. C. & B,
P. W. (1995). Regeneration and post-metamorphic development of the central nervous system in the protochordate Ciona
intestinalis : a study with monoclonal antibodies. Cell and Tissue
Research 279, 421–432.
B, Q. & B, A. C. G. (1978). Ciliated sensory cells in
amphioxus (Branchiostoma). Journal of the Marine Biological
Association, United Kingdom 58, 479–486.
B, Q. & R, K. P. (1978). Cupular sense organs in Ciona
(Tunicata : Ascideacea). Journal of Zoology 186, 417–429.
B, C. B. (1996). The sensory biology of the living jawless
fishes : a phylogenetic assessment. Brain, Behavior and Evolution
48, 262–276.
B, C. B. & N, R. G. (1997). The lateral line
system of hagfishes (Craniata : Myxinoidea). Acta Zoologica
(Stockholm) 78, 247–268.
B, C. B. & N, R. G. (1998). Cutaneous exteroreceptors and their innervation in hagfishes. In The Biology of
Hagfishes (eds. J. M. Jørgensen, J. P. Lomholt, R. E. Weber
and H. Malte), pp. 512–532. Chapman & Hall, London.
B, D. E. G., C, E. N. K. & A, R. J.
(1983). The conodont animal. Lethaia 16, 1–14.
B, D. E. G. & K, A. (1994). Decay of Branchiostoma :
implications for soft-tissue preservation in conodonts and
other primitive chordates. Lethaia 26, 275–287.
B, D. S. & D, D. L. (1973). Torpedaspis, a new
Upper Silurian and Lower Devonian genus of Cyathaspididae
(Ostracodermi) from Arctic Canada. Geological Survey of
Canada, Bulletin 222, 53–91.
B, T. H., B, D. A. & N, R. G. (1983).
The phylogenetic distribution of electroreception : evidence
for convergent evolution of a primitive vertebrate sense
modality. Brain Research Reviews 6, 25–46.
B, R. D. & H, J. C. (1992). Significance of ultrastructural features in etched conodonts. Journal of Paleontology
66, 266–276.
C, P., H, G. & G, W. J. (1997). PAX-6 in
development and evolution. Annual Review of Neuroscience 20,
483–532.
C$ , D. (1963). A crystallographic study of vertebrate
otoliths. Biological Bulletin 125, 441–463.
C-S, T. (1998). A revised six-kingdom system of
life. Biological Reviews 73, 203–266.
C, M. L. & A! --A, E. (1994). A
phylogenetic framework of the Enterocoela (Metameria :
Coelomata). Revista Nordestina de Biologia 9, 173–208.
C M, S. (1977). A redescription of the Middle
Cambrian worm Amiskwia sagittiformis Walcott from the
Burgess Shale of British Columbia. PalaW ontologische Zeitschrift
51, 271–287.
C M, S. (1989a). Conodont palaeobiology : recent
progress and unsolved problems. Terra Nova 1, 135–150.
C M, S. (1989b). The persistence of Burgess Shaletype faunas : implications for the evolution of deep-water
faunas. Transactions of the Royal Society of Edinburgh (Earth
Sciences) 80, 271–283.
Conodont affinity and chordate phylogeny
C, J. S. & P, D. F. G. (1973). The dentition and
dental tissues of the agamid lizard, Uromastyx. Journal of
Zoology 169, 85–100.
C, E. D. (1889). Synopsis on the families of the Vertebrata.
American Naturalist 23, 1–29.
C, V. M., A, R. J. & H, P. K. (1982).
Computer applications in conodont taxonomy : 1. Characterization of blade elements. In Computer Applications in Geology
I & II. Geological Society Miscellaneous Paper 14, pp. 237–246.
Geological Society of London, London.
C, V. M. & A, R. J. (1982). Computer applications
in conodont taxonomy : 2. Classificatory methods. In Computer
Applications in Geology I & II. Geological Society Miscellaneous
Paper 14, pp. 247–261. Geological Society of London, London.
C, R. J. & W, J. R. (1994). Serial repitition
of cilia pairs along the tail surface of an ascidian larva. Journal
of Experimental Zoology 268, 9–16.
D, P. G. (in press). The taphonomy of feathers. American
Zoologist
D, P. G. & B, D. E. G. (1995). Fossilization of feathers.
Geology 23, 783–786.
D, R. H. (1951). The exoskeleton of early Osteostraci.
Fieldiana Geology 11, 199–218.
D, R. H. (1964). The Cyathaspididae : a family of Silurian
and Devonian jawless vertebrates. Fieldiana Geology 13,
309–473.
D, R. H. (1967). Ordovician vertebrates from Western
United States. Fieldiana Geology 16, 131–192.
D, R. H. (1971). On the tail of Heterostraci (Agnatha).
Forma et Functio 4, 87–99.
D, R. H. (1978). Placodermi. Gustav Fisher, Stuttgart.
D Q, K. & G, J. (1992). Phylogenetic taxonomy. Annual Review of Ecology and Systematics 23, 449–480.
D, T. G. H. & V, R. (1997). Do hagfish have
teeth ? Journal of Morphology 232, 247.
D, P. C. J. (1998). Growth and patterning in the
conodont skeleton. Philosophical Transactions of the Royal Society
of London, Series B 353, 633–666.
D, P. C. J. & C, K. (1999). Conchodontus,
Mitrellataxis and Fungulodus : conodonts, fish, or both ? Lethaia
31, 283–292.
D, P. C. J. & P, M. A. (1999 a). Growth,
function, and the fossil record of conodonts. Geology 27,
251–254.
D, P. C. J. & P, M. A. (1999 b). Mammal-like
occlusion in conodonts. Paleobiology 25, 58–74.
D, P. C. J., P, M. A. & A, R. J. (1998).
Conodont anatomy, chordate phylogeny and vertebrate
classification. Lethaia 31, 211–219.
D, S. K. & P, C. R. C. (1998). The Adequacy of the
Fossil Record. John Wiley & Sons, Chichester.
D! , A. M. C. (1806). Zoologie analytique, ou meT thode naturelle
de classification des animaux. Didot, Paris.
D, J. (1986). Chordate affinities of the conodonts. In
Problematic fossil taxa. Oxford monographs on geology and geophysics
No. 5 (eds. A. Hoffman and M. H. Nitecki), pp. 240–254.
Oxford University Press, New York.
D, J. (1991). Evolution of the oral apparatuses in the
conodont chordates. Acta Palaeontologica Polonica 36, 265–323.
D, J. (1995). Yunnanozoon and the ancestry of the vertebrates.
Acta Palaeontologica Polonica 40, 341–360.
243
E, W. (1930). Conodonten aus dem Culm des Harzes.
PalaW ontologische Zeitschrift 12, 177–182.
F/ , L. E. & F/ -V R, G. E. (1987). Soft
tissue matrix of decalcified pectiniform elements of Hindeodella
confluens (Conodonta, Silurian). In Palaeobiology of conodonts
(ed. R. J. Aldridge), pp. 105–110. Ellis Horwood Ltd.,
Chichester.
F/ , L. E. & F/ -V R, G. E. (1993). Histomorphology of sectioned and stained 415 Ma old soft-tissue
matrix from internal fluorapatite skeletal elements of an
extinct taxon, Conodontophorida (Conodonta). In Structure,
Formation and Evolution of Fossil Hard Tissues (eds. I. Kobayashi,
H. Mutvei and A. Sahni), pp. 107–112. Tokai University
Press, Tokyo.
F, J. S. (1988). Hennig86, version 1.5. Program and
documentation. Port Jefferson Station, New York.
F, B. (1985). The lateral line system of cyclostomes. In
Evolutionary Biology of Primitive Fishes (eds. R. Foreman, A.
Gorbman and J. Dodd), pp. 113–122. Plenum Press, New
York.
F, B. (1998). Hagfish systematics. In The Biology of
Hagfishes (eds. J. M. Jørgensen, J. P. Lomholt, R. E. Weber
and H. Malte), pp. 33–44. Chapman & Hall, London.
F, P. L. (1995). Agnathans recent and fossil, and the origin
of jawed vertebrates. Reviews in Fish Biology and Fisheries 5,
267–303.
F, P. L. & G, B. G. (1981). J. A. Moy-Thomas and
his association with the British Museum (Natural History).
Bulletin of the British Museum (Natural History), Geology Series 35,
131–144.
F, P. L. & J, P. (1993). Agnathans and the origin of
jawed vertebrates. Nature 361, 129–134.
F, P. L. & K, I. J. (2000). Experiments in coding
multistate characters. In Homology and systematics. Coding
characters for phylogenetic analysis (eds. R. W. Scotland and
R. T. Pennington), pp. 54–80. Systematics Association Special
Volume 58. Taylor & Francis, London.
F, K. A. (in press). A taphonomic consideration of
Jamoytius kerwoodi. Palaeontology
F, W. M. (1938). Conodonts from the Prairie du Chien
(Lower Ordovician) beds of the Upper Mississippian Valley.
Journal of Paleontology 12, 318–340.
G, S. E., A, R. J. & T, J. N. (1995). A
giant conodont with preserved muscle tissue from the Upper
Ordovician of South Africa. Nature 374, 800–803.
G, P.-Y. (1989). The oldest vertebrate : a 470 million
years old jawless fish, Sacabambaspis janvieri, from the Ordovician of Bolivia. National Geographic Research 5, 250–253.
G, P.-Y. (1993a). Sacabambaspis janvieri, verte! bre! Ordovicien de Bolivie : I : analyse morphologique. Annales de
PaleT ontologie 79, 19–69.
G, P.-Y. (1993b). Sacabambaspis janvieri, verte! bre! Ordovicien de Bolivie : II : analyse phyloge! ne! tique. Annales de
PaleT ontologie 79, 119–166.
G, P.-Y. (1995). Ordovician vertebrates and agnathan
phylogeny. Bulletin du MuseT um national d’Histoire naturelle, Paris
17, 1–37.
G-F' , J. & H, P. W. H. (1994). Archetypal organisation of the amphioxus Hox gene cluster. Nature
370, 563–566.
G, M., D, S. & L, M. (1998). Evolutionary analysis of ‘ hagfish amelogenin ’. The Anatomical
Record 252, 608–611.
244
G, S., H, L. Z., G, W. J. & H,
N. D. (1998). Isolation and developmental expression of the
amphioxus Pax-6 gene (AmphiPax-6) : insights into eye and
photoreceptor evolution. Development 125, 2701–2710.
G, E. S. (1909). Cyclostomes and fishes. Part 9.
Vertebrata Craniata. In A Treatise on Zoology, (ed. E. R.
Lankester), Adam and Charles Black, London.
G, A. & T, A. (1985). Early development of
oral, olfactory and adenohypophysis structures of agnathans
and its evolutionary implications. In Evolutionary Biology of
Primitive Fishes (eds. R. E. Foreman, A. Gorbman, J. M. Dodd
and R. Olsson), pp. 165–185. Plenum Press, New York.
G, D. & Y, G. C. (1995). Interrelationships of
placoderms revisited. Geobios 19, 89–95.
G, W. (1930). Die fische des mittleren Old Red Su$ dLivlands. Geologische und palaW ontologische Abhandlungen 18.
G, W. (1957). U$ ber die basis der conodonten. PalaW ontologische
Zeitschrift 31, 78–91.
G, W. (1960). U$ ber die basis bei den gattungen Palmatolepis
und Polygnathus (Conodontida). PalaW ontologische Zeitschrift 34,
40–58.
H, K. M. (1996). Testing hypotheses of chaetognath
origins : long branches revealed by 18S ribosomal DNA.
Systematic Biology 45, 223–246.
H, B. K. (1992). The origin and evolution of vertebrate
skeletal tissues. In Chemistry and Biology of Mineralised Tissues
(eds. H. Slavkin and P. Price), pp. 103–111. Elsevier Science
Publishers,
H, B. K. (1998). Evolutionary Developmental Biology. Chapman
& Hall, London.
H, L. B. (1982). Evolutionary trends and the phylogeny
of the Agnatha. In Problems of Phylogenetic Reconstruction.
Systematics Association Special Volume 21 (eds. K. A. Joysey and
A. E. Friday), pp. 159–196. Academic Press, London.
H, L. B. (1987). Evolutionary aspects of neural crestderived skeletogenic cells in the earliest vertebrates. In
Developmental and Evolutionary Aspects of the Neural Crest (ed.
P. F. A. Maderson), pp. 339–358. John Wiley and Sons.
H T, L. B. (1964). The origin of bone. In Bone and
Tooth (ed. H. J. J. Blackwood), pp. 3–17. Pergamon Press.
H, M. W. (1979). The Biology of Cyclostomes. Chapman &
Hall, London.
H, M. W. (1982). Lampreys and hagfishes : analysis of
cyclostome relationships. In The Biology of Lampreys (eds. M. C.
Hardisty and I. C. Potter) pp. 165–259. Academic Press.
H, W. H. (1941). Morphology of conodonts. Journal of
Paleontology 15, 71–81.
H, J. A., H, C. E. & S, R. W. (1997).
Primary homology assessment, characters and character
states. Cladistics 13, 275–283.
H, A. (1939). Cephalaspida from the Downtonian of
Norway. Skrifter utgitt av det Norske Videnskaps-Akademi
(Matematiske-naturvidenskapslige Klasse) 1939, 1–119.
H, A. (1967). Some remarks about the structure of the tail
in cephalaspids. In Evolution des verteT breT s. Colloques internationaux
du Centre national de la Recherches scientifique, 104 (ed. J. P.
Lehman), pp. 13–29. Paris.
H, I., K, P., M, M. & M$ , K. J. (1990). The
problematic Hadimopanella, Kaimenella, Milaculum and Utahphospha identified as sclerites of Palaeoscolecida. Lethaia 23,
217–221.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
H, N. D., P, G., H, E. L. & H,
L. Z. (1996). Sequence and developmental expression of
AmphiDll, an amphioxus Distal-less gene transcribed ion the
ectoderm, epidermis and nervous system : insights into
evolution of craniate forebrain and neural crest. Development
122, 2911–2920.
H, P. W. H. & G-F' , J. (1996). HOX
genes and chordate evolution. Developmental Biology 173,
382–395.
H, R. (1958). Die Conodonten der Mediterranean
Trias und ihr stratigraphischer Wert. PalaW ontologische Zeitschrift
32, 141–175.
H, A. & S, J.-Y. (1998). Evolution of patterns and
processes in teeth and tooth-related tissues in non-mammalian
vertebrates. European Journal of Oral Science 106 (suppl 1),
437–481.
J, P. (1974). The sensory line system and its innervation
in the Osteostraci (Agnatha, Cephalaspidomorphi). Zoologica
Scripta 3, 91–99.
J, P. (1981). The phylogeny of the Craniata, with
particular reference to the significance of fossil ‘ agnathans ’.
Journal of Vertebrate Paleontology 1, 121–159.
J, P. (1985). Les CeT phalaspideT s du Spitsberg : anatomie,
phylogeT nie et systeT matique des OsteT ostraceT s siluro-devoniens ; revisions
des OsteT ostraceT s de la Formation de Wood Bay (DeT vonien infeT rieur du
Spitsberg). Cahiers de Pale! ontologie, Centre national de la
Recherche scientifique, Paris.
J, P. (1990). La structure de l’exosquelette des Galeaspida
(Vertebrata). Compte Rendu Academie des Sciences, Paris 310,
655–659.
J, P. (1993). Patterns of diversity in the skull of jawless
fishes. In The Skull (eds. J. Hanken and B. K. Hall), pp.
131–188. University of Chicago Press, Chicago.
J, P. (1995). Conodonts join the club. Nature 374,
761–762.
J, P. (1996 a). Early Vertebrates. Oxford University Press,
Oxford.
J, P. (1996 b). The dawn of the vertebrates : characters
versus common ascent in the rise of current vertebrate
phylogenies. Palaeontology 39, 259–287.
J, P. (1998). Les verte! bre! s avant le Silurien. Geobios 30,
931–950.
J, P. & B, A. (1979). New data on the internal
anatomy of the Heterostraci (Agnatha), with general remarks
on the phylogeny of the Craniota. Zoologica Scripta 8, 287–296.
J, P. & F, P. L. (in preparation). Introduction. In
Handbook of Paleoichthyology. Agnatha (ed. H.-P. Schultze).
Verlag Friedrich Pfeil, Mu$ nchen.
J, P. & L, R. (1983). Hardistiella montanensis n.gen. et
sp. (Petromyzontida) from the Lower Carboniferous of
Montana, with remarks on the affinities of lampreys. Journal
of Vertebrate Paleontology 2, 407–413.
J, E. (1980). Basic Structure and Evolution of Vertebrates.
Academic Press, London.
J, R. P. S. (1979). The origin of chordates : a methodological essay. In The Origin of Major Invertebrate Groups (ed.
M. R. House), pp. 1–515. Systematics Association, London.
J, L. (1979). Conodont element function. Lethaia 12,
153–171.
J, J. B. (1905). The cranial nerve components of
Petromyzon. Gegebaurs Morphologisches Jahrbuch 34, 149–203.
K-T, V. N., N, L. I., R, K.
S. & S, Z. (1990). Mongolepis – a new lower Silurian
Conodont affinity and chordate phylogeny
genus of elasmobranchs from Mongolia. Paleontologicheskii
zhurnal 1, 76–86.
K, A. P. & B, G. I. (1996 a) About the Relationship of
the Chaetognatha with Conodonts. In Sixth European Conodont
Symposium (ECOS VI) (ed. J. Dzik), p. 27. Warszawa,
Instytut Paleobiologii.
K, A. P. & B, G. I. (1996 b). On the relation of
chaetognaths and conodonts. Albertiana 18, 21–23.
K, A. P. & B, G. I. (1997). Chaetodonta : a new
animal superphylum and its position in animal systematics.
Doklady Biological Sciences 356, 503–505.
K, A. (1977). The pattern of tooth plate formation in the
Australian lungfish, Neoceratodus forsteri Krefft. Zoological
Journal of the Linnean Society 60, 223–258.
K, A. & N, R. S. (1995 a) On Conodont and Vertebrate
Hard Tissues. In Proceedings of the 10th International
Symposium on Dental Morphology (eds. R. J. Radlanski and
H. Renz), pp. 7–12. Berlin, ‘ M ’-Marketing Services.
K, A. & N, R. S. (1995 b). Protochordate affinities of
conodonts. Courier Forschungsinstitut Senckenberg 182, 235–245.
K, A. & N, R. S. (1996). Histology and histochemistry
of conodont elements. Modern Geology 20, 287–302.
K, R., G, R. C., N, H., K, H.,
K, T. & A, F. (1987). Primary neurons of the
lateral line nerves and their central projections in hagfishes.
Journal of Comparative Neurology 264, 303–310.
K, G. & F, J. C. T. (1986). Quantification of
outlines in Frasnian (Upper Devonian) platform conodonts.
Canadian Journal of Earth Sciences 23, 1214–1222.
K, G. & F J., C. T. (1993). Shape analysis of
Frasnian species of the Late Devonian conodont genus
Palmatolepis. Paleontological Society Memoir 32, 1–35.
K, H. (1972). The sense organs. In The Biology of
Lampreys (eds. M. W. Hardisty and I. C. Potter). Academic
Press, London.
K, E. J. (1998). Odontogenesis : a retrospective. European
Journal of Oral Science 106 (suppl 1), 2–6.
K, E. J. & F, C. (1980). Tooth induction in chick
epithelium : expression of quiescent genes for enamel synthesis.
Science 207, 993–885.
K, P. & M, M. (1989). Worm-like fossils (Palaeoscolecida ; ?Chaetognatha) from the Lower Ordovician of
Bohemia. Sbornik geologickych ved. Paleontologie 30, 9–36.
K, R. J., B, P. & S, H. C. (1990 a). The
cyclostome model : an interpretation of conodont element
structure and function based on cyclostome tooth morphology, function, and life history. Courier Forschungsinstitut
Senckenberg 118, 473–492.
K, R. J., B, P. & S, H. C. (1990 b). A
neontological interpretation of conodont elements based on
agnathan cyclostome tooth structure, function, and development. Lethaia 23, 359–378.
K, A. (1853). Nachtra$ gliche Bermerkungen u$ ber den Bau
der Gattung Sagitta, nebst der Beschreibung einiger neuen
Arten. Archiv fuW r Naturgesch XIX, 266–281.
L, T. C. (1996). Frontal eye circuitary, rostral sensory
pathways and brain organisation in amphioxus larvae :
evidence from 3D reconstructions. Philosophical Transactions of
the Royal Society of London, Series B 351, 243–263.
L, T. C., H, N. D. & W, J. E. (1994).
Landmarks in the anterior central nervous system of
amphioxus larvae. Philosophical Transactions of the Royal Society
of London, Series B 344, 165–185.
245
L, G., P, A., L, P. & V, G.
(1994). Ancestral hemoglobin switching in lampreys. Developmental Biology 164, 402–408.
L, R. M. & H, B. K. (1993). Calcification of
cartilage from the lamprey Petromyzon marinus (L.) in vitro. Acta
Zoologica (Stockholm) 74, 31–41.
L, E. R. (1868–70). A Monograph of the Fishes of the Old
Red Sandstone of Britain. 1. The Cephalaspidae. Palaeontographical Society, London.
L$ , M. (1964). Conodonts. Elsevier, Amsterdam.
L$ , M. & Z, W. (1971). Feinstrukturelle untersuchungen an conodonten 1. Die u$ berfamilie Panderodontacea. Geologica et Palaeontologica 5, 9–33.
L, C. (1758). Systema naturae per regna tria naturae (10th
edn). Laurentii Salvii, Stockholm.
L, D. L., F, J. S., K$ , M. & T, A.
(1998). Support, ribosomal sequences and the phylogeny of
the eukaryotes. Cladistics 14, 303–338.
L, D. T. J., T, M. J., C, K. A. &
R, K. (1998). Gnathostomulida – an enigmatic
metazoan phylum from both morphological and molecular
perspectives. Molecular Phylogenetics and Evolution 9, 72–79.
L, S. (1977). The Phylogeny of the Vertebrata. Wiley, New
York.
L, H. A. (1981). Minerals formed by organisms.
Science 211, 1126–1131.
L, R. & J, P. (1986). A second lamprey from the
Lower Carboniferous (Namurian) of Bear Gulch, Montana
(U.S.A.). Geobios 19, 647–652.
M, G. O. (1995). On the ‘ visceral nervous system ’ of
Ciona. Journal of the Marine Biological Association of the U.K. 75,
141–151.
M, J. G. (1986). Head and tails : a chordate phylogeny.
Cladistics 2, 201–256.
M, J. G. (1988). Phylogeny of early vertebrate skeletal
induction and ossification patterns. Evolutionary Biology 22,
1–36.
M, J. (1997a). Crossing a major morphological boundary : the origin of jaws in vertebrates. Zoology 100, 128–140.
M, J. (1997b). Shark pharyngeal muscles and early
vertebrate evolution. Acta Zoologica (Stockholm) 78, 279–294.
M, J. & S, J. (1998). 28S and 18S rDNA
sequences support the monophyly of lampreys and hagfishes.
Molecular Biology and Evolution 15, 1706–1718.
M$ , T. (1979). Lateral line sensory system of the ludlovian
thelodont Phlebolepis elegans Pander. Proceedings of the Estonian
Academy of Sciences : Geology 1979, 108–111.
M, D. G., B, D. E. G. & K, J. (1985 a). A
new exceptionally preserved biota from the Lower Silurian of
Wisconsin, USA. Philosophical Transactions of the Royal Society of
London, Series B 311, 78–85.
M, D. G., B, D. E. G. & K, J. (1985 b). A
Silurian soft-bodied biota. Science 228, 715–717.
M, J. F. (1969). Conodont fauna of the Notch Peak
Limestone (Cambro-Ordovician), House Range, Utah.
Journal of Paleontology 43, 413–439.
M, J. F. (1980). Taxonomic revisions of some Upper
Cambrian and Lower Ordovician conodonts with comments
on their evolution. University of Kansas Paleontological Contributions 99, 1–44.
M, J. F. (1984). Cambrian and earliest Ordovician
conodont evolution, biofacies, and provincialism. In Conodont
246
Biofacies and Provincialism (ed. D. L. Clark), pp. 43–68.
Geological Society of America, Boulder.
M, M. L. (1964). The phylogeny of mineralised tissues. Int.
Rev. Gen. Exp. Zool. 1, 297–331.
M-T, J. A. & M, R. S. (1971). Palaeozoic Fishes.
Chapman & Hall, London.
M$ , K. J. (1981). Zoological affinities. In Treatise on
Invertebrate Paleontology, Part W, Miscellanea, Supplement 2,
Conodonta (ed. R. A. Robison), pp. 78–82. Geological Society
of America and University of Kansas, Lawrence.
M$ , K. J. & H-S, I. (1993). Palaeoscolecid worms from the Middle Cambrian of Australia.
Palaeontology 36, 549–592.
M$ , K. J. & H-S, I. (1998). Internal
structure of Cambrian conodonts. Journal of Paleontology 72,
91–112.
M$ , K. J. & N, Y. (1971). U$ ber die Feinbau der
Conodonten. Memoirs of the Faculty of Science, Kyoto University,
Series of Geology and Mineralogy 38, 1–87.
M$ , K. J. & N, Y. (1972). Growth and Function of
Conodonts. In 24th International Geological Congress, 7, pp.
20–27. Montreal.
M, M. A. & C, M. K. (1986). Statistical study
of Ozarkodina excavata (Branson and Mehl) and O. tuma
Murphy and Matti (Lower Devonian, delta zone, conodonts,
Nevada. Journal of Paleontology 60, 865–869.
M, M. A. & C, M. K. (1987). Morphometric
study of the genus Ancyrodelloides (Lower Devonian, conodonts), central Nevada. Journal of Paleontology 61, 583–594.
M, M. A. & M, J. C. (1982). Lower Devonian
conodonts [hesoerius-kindlei zones] central Nevada. University of
California Publications in Geological Sciences 123, 1–83.
M, L. E. (1993). Evolution of gonadotropin-releasing
hormone (GnRH) neuronal systems. Brain, Behavior and
Evolution 42, 215–230.
N, C. H. & N, Y. (1978). Determination of
the embryonic origin of the mesencephalic nucleus of the
trigeminal nerve in birds. Journal of Embryology and Experimental
Morphology 43, 85–105.
N, G. J. (1972). Comments on Hennig’s ‘ Phylogenetic
systematics ’ and its influence on ichthyology. Systematic Zoology
21, 364–374.
N, J. S. (1994). Fishes of the World. Wiley, New York.
N, C. (1995). Animal Evolution : Interrelationships of the Living
Phyla. Oxford University Press, New York.
N, C., S, N. & E-J, D. (1996).
Cladistic analysis of the animal kingdom. Biological Journal of
the Linnean Society 57, 385–410.
N, R. G. (1981). Evolution of the telencephalon in
nonmammals. Annual Review of Neuroscience 4, 301–350.
N, R. G. (1985). The brain and sense organs of the
earliest vertebrates : reconstruction of a morphotype. In
Evolutionary Biology of Primitive Fishes (eds. R. E. Foreman, A.
Gorbman, J. M. Dodd and R. Olsson), pp. 81–112. Plenum
Press, New York.
N, R. G. (1989). The phylogenetic distribution and
innervation of craniate mechanoreceptive lateral lines. In The
Mechanosensory Lateral Line : Neurobiology and Innervartion (eds. S.
Coombs, P. Go$ rner and H. Mu$ nz), pp. 17–78. SpringerVerlag, New York.
N, R. G. (1996 a). The agnathan ark : the origin of
craniate brains. Brain, Behavior and Evolution 48, 237–247.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
N, R. G. (1996 b). The origin of craniates : neural
crest, neurogenic placodes, and homeobox genes. Israel Journal
of Zoology 42, 273–313.
N, R. G. (1997). Evolution of gnathostome lateral line
ontogenies. Brain, Behavior and Evolution 50, 25–37.
N, R. G., B$ , K. & F, B. (1995).
Electroreceptors and mechanosensory lateral line organs arise
from single placodes in axolotls. Developmental Biology 168,
358–373.
N, R. G., C, K. C. & C, B. B. (1994).
Development of the lateral line organs in the axolotl. Journal
of Comparative Neurology 340, 480–514.
N, R. G. & G, C. (1983). The genesis of neural
crest and epidermal placodes : a reinterpretation of vertebrate
origins. Quarterly Review of Biology 58, 1–28.
N, L. I. & T, S. (1998). Turinia pagei (Powrie) :
a new reconstruction of the soft organs of the cephalothorax.
Memoirs of the Queensland Museum 42, 533–544.
Ø, T. (1951). Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 1. The endoskeleton, with
remarks on the hard tissues of lower vertebrates in general.
Arkiv foW r Zoologi 2, 321–454.
Ø, T. (1958). Pycnaspis splendens, new genus, new species, a
new ostracoderm from the Upper Ordovician of North
America. Proceedings of the United States National Museum 108,
1–23.
Ø, T. (1965). Palaeohistological notes 2 : certain comments
on the phylogenetic significance of acellular bone in early
lower vertebrates. Arkiv foW r Zoologi 16, 551–556.
Ø, T. (1967). Phylogeny of tooth tissues : evolution of some
calcified tissues in early vertebrates. In Structural and Chemical
Organisation of Teeth (ed. A. E. W. Miles), pp. 45–110.
Academic Press, London.
Ø, T. (1971). Comments on the lateral line system of some
brachythoracid and ptyctodontid arthrodires. Zoologica Scripta
1, 5–35.
Ø, T. (1973). Acanthodian dentition and its bearing on the
relationships of the group. Palaeontographica (Abt. A) 143,
119–150.
Ø, T. (1989). Histologic studies of ostracoderms, placoderms and fossil elasmobranchs 6. Hard tissues of Ordovician
vertebrates. Zoologica Scripta 18, 427–446.
O, J. W. (1984). From reptile to mammal : evolutionary
considerations of the dentition with emphasis on tooth
attachment. Symposia of the Zoological Society of London 52,
549–574.
O, J. W. & P, D. G. (1988). An autoradiographic
study of periodontal development in the mouse. Journal of
Dental Research 67, 455–461.
P, R. M. & L, A. G. S. (1987). Development of
periodontal ligament and aveolar bone in homografted
recombinations of enamel organs and papillary, pulpal and
follicular mesenchyme in the mouse. Archives of Oral Biology 32,
281–289.
P, C. H. (1856). Monographie der fossilen Fische des silurischen
Systems der russischbaltischen Gouvernements. Akademie der Wissenschaften, St Petersburg.
P, L. R. (1986). The phylogenetic significance of bone
types in euteleost fishes. Zoological Journal of the Linnean Society
87, 37–51.
P, C. (1993). Naming names. Nature 366, 518.
Conodont affinity and chordate phylogeny
P, C. & R, D. E. (1977). Review of ichthyodectiform and other Mesozoic Teleost fishes and the theory
and practice of classifying fossils. Bulletin of the American
Museum of Natural History 158, 83–172.
P, K. J. (1994). The origin and early evolution of the
Craniata. In Major Features of Vertebrate Evolution (eds. D. R.
Prothero and R. M. Schoch), pp. 14–37. The Paleontological
Society.
P, H., C, A. & A, A. (1994). Can the
Cambrian explosion be inferred through molecular phylogeny. Development (Supplement) 15–25.
P, R. A. & R, R. (1987). The nature of cladistic
data. Cladistics 3, 275–289.
P, N. I., G, C. E. & C, J. A. (1991).
On missing entries in cladistic analysis. Cladistics 7, 337–343.
P, F. (1995). On character coding for phylogeny
reconstruction. Cladistics 11, 309–315.
P, H., R, W.-E. & M$ , W. H. (1974). Funktionsanpassungen in form und struktur an haifischza$ hnen.
Zeitschrift fuW r Anatomie und Entwickelungsgeschichte 143, 315–344.
P, P. (1974). The function of conodonts. Geological
Magazine 111, 255–257.
P, P. A., B, R. E. & N, R. S. (1997). Soft
anatomy and affinities of conodonts. Lethaia 29, 317–328.
P, M. A. (1995). Microwear on conodont elements and
macrophagy in the first vertebrates. Nature 374, 798–800.
P, M. A. & D, P. C. J. (1997). Skeletal architecture and functional morphology of ozarkodinid conodonts.
Philosophical Transactions of the Royal Society of London, Series B
352, 1545–1564.
P, M. A. & D, P. C. J. (1998). Architecture
and functional morphology of the skeletal apparatus of
ozarkodinid conodonts. Palaeontology 41, 57–102.
P, M. A., D, P. C. J. & A, R. J. (2000).
Orientation and anatomical notation in conodonts. Journal of
Paleontology 74, 113–122.
R, R. A. (1996). The Shape of Life : Genes, Development, and the
Evolution of Animal Form. University of Chicago Press, London.
R, W.-E. (1973). Morphologie und ultrastruktur des hai‘ schmelzes ’. Zoologica Scripta 2, 231–250.
R, W.-E. (1979). Structural convergences between enameloid
of Actionpterygian teeth and of shark. Scanning Electron
Microscopy 1979, 547–554.
R, W.-E. (1981). Biomechanik von hai- und teleosteerza$ hnen. PalaW ontologische KursbuW cher, band 1 : Funktionsmorphologie
1, 71–83.
R, W. E. (1982). Evolution of dermal skeleton and dentition
in vertebrates : The odontode regulation theory. Evolutionary
Biology 15, 287–368.
R, F. H. T. (1954). The zoological affinities of the
conodonts. Biological Reviews 29, 419–452.
R, F. H. T., W, J. A. & R, J. C. (1973).
Micromorphologic studies of platform conodonts. In Conodont
Paleozoology (ed. F. H. T. Rhodes), pp. 117–141. Geological
Society of America, Boulder, Colorado
R, E. S. (1982). Problematica of the Mazon Creek
(Pennsylvanian, Westphalian D, Illinois). Journal of
Paleontology 56 Suppl, 22.
R, S. (1973). Zur Deutung der Conodonten. Natur und
Museum 103, 409–418.
R, A. (1960). A new interpretation of Jamoytius kerwoodi
White. Nature 188, 647–649.
247
R, A. (1968). New evidence on Jamoytius kerwoodi White,
an important ostracoderm from the Silurian of Lanarkshire,
Scotland. Palaeontology 11, 21–39.
R, A. (1984). Conflicting interpretations of the Silurian
agnathan Jamoytius. Scottish Journal of Geology 20, 249–256.
R, A. & G-T, J. (1977). First Ordovician
vertebrates from the Southern Hemisphere. Alcheringa 1,
351–368.
R, M. & N, R. G. (1987). Primary projections of
the lateral line nerves in adult lampreys. Brain, Behavior and
Evolution 30, 62–81.
R, M. & N, R. G. (1998). The central nervous
system of hagfishes. In The Biology of Hagfishes (eds. J. M.
Jørgensen, J. P. Lomholt, R. E. Weber and H. Malte), pp.
452–479. Chapman & Hall, London.
S, D. & R, P. (1975). Locating the vertices of a
Steiner tree in an arbitrary space. Mathematical Progress 9,
240–246.
S, I. J. (1996). Pseudooneotodus : a histological study of an
Ordovician to Devonian vertebrate lineage. Zoological Journal
of the Linnean Society 118, 47–57.
S, I. J., A, H. A. & S, M. P. (1994 a). The
apparatus architecture of Panderodus and its implications for
coniform conodont classification. Palaeontology 37, 781–799.
S, I. J., S, M. P., A, H. A. & S, M. M.
(1992). Presence of the earliest vertebrate hard tissues in
conodonts. Science 256, 1308–1311.
S, I. J., S, M. P. & S, M. M. (1994 b). Dentine in
conodonts. Nature 368, 591.
S, I. J., S, M. P., S, M. M. & T, P.
(1997). Astraspis – the anatomy and histology of an Ordovician fish. Palaeontology 40, 625–643.
S, B. (1977). The dermal skeleton in fishes. In Problems
in Vertebrate Evolution (eds. S. Mahala Andrews, R. S. Miles
and A. D. Walker), pp. 25–54. Linnean Society Symposium
4, Academic Press, London.
S, H. & M$ , K. J. (1964). Weitere Funde von
Conodonten-Gruppen aus dem oberen Karbon des
Sauerlandes. PalaW ontologische Zeitschrift 38, 105–135.
S, H.-P. (1996). Conodont histology : an indicator of
vertebrate relationship ? Modern Geology 20, 275–286.
S, A. C., S, S. M. & H, P. W. H. (1999).
An amphioxus Msx gene expressed predominantly in the
dorsal neural tube. Development, Genes and Evolution 209,
260–263.
S, R. P. & M, A. E. W. (1974). Autoradiographic
study of the formation of enameloid and dentine matrices in
teleost fishes using tritiated amino acids. Proceedings of the Royal
Society of London, Series B 185, 51–72.
S, H. C. & D, T. G. H. (1996). Evolution in
tooth developmental biology : of morphology and molecules.
The Anatomical Record 245, 131–150.
S, H. C. & D, T. G. H. (1997). Molecular
strategies of tooth enamel formation are highly conserved
during vertebrate evolution. In Dental Enamel (eds. D. J.
Chadwick and G. Cardew), pp. 73–84. Ciba Foundation
Symposium 205. John Wiley & Sons, Chichester.
S, H. C., G, E., Z-D, M. &
H, W. (1983). Enamel-like antigens in hagfish :
possible evolutionary significance. Evolution 37, 404–412.
S, A. B. (1994). Systematics and the Fossil Record : Documenting
Evolutionary Patterns. Blackwell Scientific, Oxford.
248
S, I. C. (1957). New restorations of the heads of Pharyngolepis
oblongus Kiaer and Pharyngolepis kiaeri sp. nov., with a note on
their lateral-line systems. Norsk Geologisk Tiddskrift 37,
373–402.
S, M. M. (1989). Distribution and variation in enamel
structure in the oral teeth of Sarcopterygians : its significance
for the evolution of a protoprismatic enamel. Historical Biology
3, 97–126.
S, M. M. (1991). Putative skeletal neural crest cells in early
Late Ordovician vertebrates from Colorado. Science 251,
301–303.
S, M. M. (1992) Microstructure and evolution of enamel
amongst osteichthyan and early tetrapods. In Structure,
Function and Evolution of Teeth, Proceedings of the 8th International symposium on dental morphology (ed. P. Smith),
pp. 73–101. Jerusalem, Israel.
S, M. M. (1995). Heterochrony in the evolution of enamel
in vertebrates. In Evolutionary Change and Heterochrony (ed.
K. J. McNamara), pp. 125–150. John Wiley & Sons.
S, M. M. & C, M. I. (1998). Evolutionary origins of
the vertebrate dentition : phylogenetic patterns and developmental evolution. European Journal of Oral Science 106
(suppl. 1), 482–500.
S, M. M. & H, B. K. (1990). Development and
evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biological Reviews 65, 277–373.
S, M. M. & H, B. K. (1993). A developmental model
for evolution of the vertebrate exoskeleton and teeth : the role
of cranial and trunk neural crest. Evolutionary Biology 27,
387–448.
S, M. M. & S, I. J. (1997). Exoskeletal microremains
of an Ordovician fish from the Harding Sandstone of
Colorado. Palaeontology 40, 645–658.
S, M. M., S, I. J. & S, M. P. (1995). Diversity of
the dermal skeleton in Ordovician to Silurian vertebrate taxa
from North America : histology, skeletogenesis and relationships. Geobios 19, 65–70.
S, M. M., S, I. J. & S, M. P. (1996). ‘ Teeth ’
before armour : the earliest vertebrate mineralized tissues.
Modern Geology 20, 303–319.
S, M. P., B, D. E. G. & A, R. J. (1987). A
conodont animal from the lower Silurian of Wisconsin,
U.S.A., and the apparatus architecture of panderodontid
conodonts. In Palaeobiology of Conodonts (ed. R. J. Aldridge),
pp. 91–104. Ellis Horwood, Chichester.
S, S. C., G, A. C. & H, B. K. (1994). Evidence
for a developmental and evolutionary link between placodal
ectoderm and neural crest. Journal of Experimental Zoology 270,
292–301.
S, K. L. & W, M. V. H. (1990). A complete,
articulated heterostracan from the Wenlockian (Silurian)
beds of the Delorme Group, Mackenzie Mountains,
Northwest Territories, Canada. Journal of Vertebrate Paleontology 10, 405–419.
S, C. R. & P, H. J. (1932). Texas Pennsylvanian
conodonts and their stratigraphic relations. University of Texas
Bulletin 3201, 13–50.
S$ , E. A. (1927). The Downtonian and Devonian
vertebrates of Spitsbergen. Part 1. Family Cephalaspidae.
Skrifter om Svalbard og Nordishavet 12, 1–391.
S$ , E. A. (1964). Les cyclostomes fossiles ou ostracodermes.
In (ed. J. Piveteau) TraiteT de paleT ontologie, v. 4, pp. 96–382.
Masson, Paris.
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
S$ , E. A. (1968). The cyclostomes, with special reference to
the diphyletic origin of the Petromyzontida and Myxinoidea.
In Current Problems in Lower Vertebrate Phylogeny, Nobel Symposium
4 (ed. T. Ørvig), pp. 13–71. Almquist & Wiksell, Stockholm.
S, D. W. & W, G. S. (1992). Evidence from 18S
ribosomal RNA sequences that lampreys and hagfishes form a
natural group. Science 257, 787–789.
S, M., K, K., N, H. & U, A.
(1995). Sequence analysis of vasotocin cDNAs of the lamprey
Lampetra japonica, and the hagfish, Eptatretus burgeri : evolution
of cyclostome vasotocin precursors. Journal of Molecular
Endocrinology 14, 67–77.
S, W. C. (1981). Macromorphology of elements and
apparatuses. In Treatise on Invertebrate Paleontology, Part W,
Miscellanea, Supplement 2, Conodonta (ed. R. A. Robison), pp.
W5–W20. Geological Society of America and the University
of Kansas Press, Boulder, Colorado and Lawrence, Kansas,
Lawrence.
S, W. C. (1988). The Conodonta : Morphology, Taxonomy,
Paleoecology, and Evolutionary History of a Long-extinct Animal
Phylum. Clarendon Press, Oxford.
S, W. C. & S$ , H. P. (1975). Conodonts of the
genus Oulodus Branson & Mehl, 1933. Geologica et Palaeontologica 9, 41–59.
S, D. L. (1993). PAUP, Phylogenetic analysis using
parsimony, version 3.1. Illinois Natural History Survey,
Champaign.
S, H. (1982). Chaetognath grasping spines recognised
among Cambrian protoconodonts. Journal of Paleontology 56,
806–810.
S, H. (1983). Structure of protoconodont elements.
Fossils and Strata 15, 21–27.
S, H. (1987). Preliminary structural comparisons of
protoconodont, paraconodont, and euconodont elements. In
Palaeobiology of Conodonts (ed. R. J. Aldridge), pp. 35–47. Ellis
Horwood, Chichester.
S, H. & B, S. (1993). Origin of euconodont
elements. Journal of Paleontology 67, 640–654.
T, M. J. & H, P. W. H. (1993). The phylogenetic
affinities of the chaetognaths : a molecular analysis. Molecular
Biology and Evolution 10, 660–676.
T C, A. R. (1975). Formation of supporting bone in
association with periodontal ligament organisation in the
mouse. Archives of Oral Biology 20, 137–138.
T C, A. R. & M, S. C. (1972). Development of
periodontium – origin of alveolar bone. The Anatomical Record
173, 69–78.
T, K. S. (1977). On the individual history of cosmine
and a possible electroreceptive function of the pore-canal
system in fossil fishes. In Problems in Vertebrate Evolution (eds.
S. M. Andrews, R. S. Miles and A. D. Walker), pp. 247–271.
Academic Press, London.
T, S. A. & C, R. A. (1982). Nervous system of
ascidian larvae : caudal primary sensory neurons. Zoomorphology 99, 103–115.
T, K. M. (1980). Preserved organic ultrastructure : an
unreliable indicator for Paleozoic amino acid biogeochemistry. In Biogeochemistry of Amino Acids (eds. P. E. Hare,
T. C. Hoering and K. King jr.), pp. 65–74. John Wiley &
Sons.
T, R. H. (1899). Report on the fossil fishes collected by
the Geological Survey of Scotland in the Silurian rocks of the
Conodont affinity and chordate phylogeny
249
south of Scotland. Transactions of the Royal Society of Edinburgh
39, 827–864.
T, J. M., S, J. R. & R, R. A. (1994).
Deuterostome phylogeny and the sister group of the chordates
– evidence from molecules and morphology. Molecular Biology
and Evolution 11, 648–655.
T, S. (1991). Monophyly and interrelationships of the
Thelodonti. In Early Vertebrates and Related Problems of
Evoltionary Biology (ed. M.-M. Chang, Y.-H. Liu and G.-R.
Zhang), pp. 87–119. Science Press, Beijing.
. K, W. (1997). Evolutionary trends in the
differentiation of mammalian enamel ultrastructure. In Tooth
Enamel Microstructure (eds. W. v. Koenigswald and P. M.
Sander), pp. 203–235. A. A. Balkema, Rotterdam.
W, H., S, H., S, N. & H, P. W. H. (1998).
Tripartite organization of the ancestral chordate brain and
the antiquity of placodes : insights from ascidian Pax-2\5\8,
Hox and Otx genes. Development 125, 1113–1122.
W, H. & S, N. (1994). Details of the evolutionary
history from invertebrates to vertebrates, as deduced from the
sequences of 18S rDNA. Proceedings of the National Academy of
Sciences, USA 91, 1801–1804.
W, O. H. (1964). Conodonten des Silurs. Abhandlungen
hessisches Landesamt fuW r Bodenforschung, Wiesbaden 41, 1–106.
W, N. Z. (1991). Two new galeaspids (jawless craniates)
from Zhejiang Province, China, with a discussion of galeaspidgnathostome relationships. In Early Vertebrates and Related
Problems in Evolutionary Biology (eds. M.-M. Chang, Y.-H. Liu
and G.-R. Zhang), pp. 41–65. Science Press, Beijing.
W$ , G. (1952). The Downtonian and Devonian
vertebrates of Spitsbergen. IX. Morphologic and systematic
studies of the Spitsbergen cephalaspids. Norsk Polarinstitutt
Skrifter 97, 1–615.
W, G. F. (1966). The Middle and Upper Ordovician
conodont faunas of Minnesota. Minnesota Geological Survey,
Special Publication Series SP-4, 1–123.
W, C. & N, R. G. (1998). To the phylogenetic
origin of the cerebellum : tracing studies on the Silver Lamprey
Ichthyomyzon unicuspis. European Journal of Neuroscience 10,
Suppl. 10, 196.
W, E. I. (1946). Jamoytius kerwoodi, a new chordate from the
Silurian of Lanarkshire. Journal of Geology 83, 89–97.
W, H. (1996). The brains of lampreys and hagfishes :
characteristics, characters, and comparisons. Brain, Behavior
and Evolution 48, 248–261.
W, H. & N, R. G. (1992). The forebrain of the
Pacific hagfish : a cladistic reconstruction of the ancestral
craniate forebrain. Brain, Behavior and Evolution 40, 25–64.
W, H. & N, R. G. (1995). Ontogeny of the head
of the Pacific hagfish (Eptatretus stouti, Myxinoidea) : development of the lateral line system. Philosophical Transactions
of the Royal Society of London, Series B 349, 119–134.
W, E. O. (1979). An annotated Linnean hierarchy, with
comments on natural taxa and competing systems. Systematic
Zoology 28, 308–337.
W, M. (1995). A comparison of two methods of
character construction. Cladistics 11, 297–308.
W, M. V. H. & C, M. W. (1993). New Silurian
and Devonian fork-tailed ‘ thelodonts ’ are jawless vertebrates
with stomachs and deep bodies. Nature 361, 442–444.
W, M. V. H. & C, M. W. (1998). The
Furcacaudiformes : a new order of jawless vertebrates with
thelodont scales, based on articulated Silurian and Devonian
fossils from Northern Canada. Journal of Vertebrate Paleontology
18, 10–29.
W, M. V. H. & S, K. L. (1990). Discovery of
complete Silurian fish. Oldest heterostracan tail has dermal
fin ‘ rays ’. Naturwissenschaften 77, 328–330.
Y, D. W. (1985). Feeding mechanisms as evidence of
cyclostome monophyly. Zoological Journal of the Linnean Society
84, 291–300.
Y, G. C. (1991). The first armoured agnathan vertebrates
from the Devonian of Australia. In Early Vertebrates and Related
Problems in Evolutionary Biology (eds. M.-M. Chang, Y.-H. Liu
and G.-R. Zhang), pp. 67–85. Science Press, Beijing.
Y, G. C. (1997). Ordovician mircovertebrate remains from
the Amadeus Basin, central Australia. Journal of Vertebrate
Paleontology 17, 1–25.
Y, G. C., K-T, V. N. & S, M. M.
(1996). A possible Late Cambrian vertebrate from Australia.
Nature 383, 810–812.
Z, M. & J, P. (1998). The histological structure of the
endoskeleton in galeaspids (Galeaspida, Vertebrata). Journal
of Vertebrate Paleontology 18, 650–654.
Z! , J., M, S., K, P., B) , A. & T, D.
(1998). Phylogeny of the Metazoa based on morphological
and 18S ribosomal DNA evidence. Cladistics 14, 249–285.
XI. APPENDIX
(1) Character diagnostics
Character statistics for the tree presented in Fig. (7A). Guide to abbreviations : CI, consistency index, HI,
homoplasy index, RI, retention index, RC, rescaled consistency index.
Appendix.
Character
1.
2.
3.
4.
5.
6.
Minimum
Steps
Tree
Steps
Maximum
Steps
CI
HI
RI
RC
1
1
1
2
1
2
1
1
2
3
1
2
2
2
3
3
2
3
1.000
1.000
0.500
0.667
1.000
1.000
0.000
0.000
0.500
0.333
0.000
0.000
1.000
1.000
0.500
0.000
1.000
1.000
1.000
1.000
0.250
0.000
1.000
1.000
P. C. J. Donoghue, P. L. Forey and R. J. Aldridge
250
Appendix. (cont.)
Character
Minimum
Steps
Tree
Steps
Maximum
Steps
CI
HI
RI
RC
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
1
1
1
1
1
1
1
2
1
1
2
2
1
3
1
1
1
1
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
2
2
1
1
3
2
2
4
2
1
3
1
1
1
1
3
3
2
1
3
3
1
2
2
1
2
2
1
1
1
3
1
1
3
2
3
1
2
2
3
2
1
2
2
2
1
2
1
1
2
4
1
2
2
2
2
4
2
3
5
3
3
4
4
3
3
2
4
7
3
2
7
6
2
3
2
3
3
2
3
3
2
3
3
2
4
4
5
2
3
2
6
3
2
3
2
3
3
2
2
3
1.000
1.000
1.000
0.500
0.500
1.000
1.000
0.667
0.500
0.500
0.500
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.667
0.667
0.500
1.000
0.333
0.333
1.000
0.500
0.500
1.000
0.500
0.500
1.000
1.000
1.000
0.333
1.000
1.000
0.333
0.500
0.333
1.000
0.500
0.500
0.667
0.500
1.000
0.500
0.500
0.500
1.000
0.500
1.000
1.000
0.000
0.000
0.000
0.500
0.500
0.000
0.000
0.333
0.500
0.500
0.500
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.333
0.333
0.500
0.000
0.667
0.667
0.000
0.500
0.500
0.000
0.500
0.500
0.000
0.000
0.000
0.667
0.000
0.000
0.667
0.500
0.667
0.000
0.500
0.500
0.333
0.500
0.000
0.500
0.500
0.500
0.000
0.500
0.000
0.000
1.000
1.000
0\0
0.000
0.000
1.000
1.000
0.500
0.000
0.500
0.333
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.500
0.800
0.500
1.000
0.667
0.600
1.000
0.500
0.000
1.000
0.500
0.000
1.000
1.000
1.000
0.000
1.000
1.000
0.333
0.667
0.500
1.000
0.500
0.000
0.750
0.500
1.000
0.500
0.000
0.500
1.000
0.000
1.000
1.000
1.000
1.000
0\0
0.000
0.000
1.000
1.000
0.333
0.000
0.250
0.167
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.333
0.533
0.250
1.000
0.222
0.200
1.000
0.250
0.000
1.000
0.250
0.000
1.000
1.000
1.000
0.000
1.000
1.000
0.111
0.333
0.167
1.000
0.250
0.000
0.500
0.250
1.000
0.250
0.000
0.250
1.000
0.000
1.000
1.000
Conodont affinity and chordate phylogeny
251
Appendix. (cont.)
Character
Minimum
Steps
Tree
Steps
Maximum
Steps
CI
HI
RI
RC
59.
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
92.
93.
94.
95.
96.
97.
98.
99.
100.
101.
102.
103.
1
1
1
1
1
1
1
1
1
1
2
2
1
1
2
2
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
1
2
1
2
3
2
5
3
3
1
3
3
1
3
3
4
1
1
2
3
1
1
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
2
2
1
2
3
3
3
5
3
5
3
3
6
2
6
4
6
2
6
9
3
5
3
9
2
2
4
3
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
1.000
1.000
0.500
1.000
1.000
0.500
1.000
0.500
0.333
0.500
0.400
0.667
0.333
1.000
0.667
0.667
1.000
0.333
0.333
0.500
1.000
1.000
0.500
0.333
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.500
1.000
1.000
1.000
1.000
0.500
0.500
1.000
0.500
0.000
0.000
0.500
0.000
0.000
0.500
0.000
0.500
0.667
0.500
0.600
0.333
0.667
0.000
0.333
0.333
0.000
0.667
0.667
0.500
0.000
0.000
0.500
0.667
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.500
0.000
0.000
0.000
0.000
0.500
0.500
0.000
0.500
1.000
1.000
0.500
1.000
1.000
0.750
1.000
0.500
0.600
0.000
0.250
0.500
0.600
1.000
0.750
0.857
1.000
0.500
0.000
0.714
1.000
1.000
0.667
0.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.000
1.000
1.000
1.000
1.000
0.000
0.000
1.000
0.000
1.000
1.000
0.250
1.000
1.000
0.375
1.000
0.250
0.200
0.000
0.100
0.333
0.200
1.000
0.500
0.571
1.000
0.167
0.000
0.357
1.000
1.000
0.333
0.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
0.000
1.000
1.000
1.000
1.000
0.000
0.000
1.000
0.000