%oo/o,~zc~i/Journal
o f t h e Linnean Society (1982), 74: 35-67. With 10 figures
Primitive bony fishes, with especial
reference to CheiroZepis and
palaeonisciform actinopterygians
D. M . PEARSON
Department $Geology, The UniversityofNewcastle-upon-Tyne,
Newcastle-upon-TyneNEl7RU"
Acceptedforpublication March I98 I
The relationships of the Devonian palaeonisciform fish Cheirolepzs are examined and the early
evolutionary trends within the Actinopterygiiand the Osteichthyesare considered.
Cherrolepts is the most primitive known actinopterygian. The contemporary stegotrachelid
palaeonisciforms are more advanced in their cranial and locomotor anatomy. The general directions
of these advances are similar to those subsequently displayed by later palaeonisciforms over the
stegotrachelids themselves. Cheiroolepis, furthermore, possesses many characters which can be logically
interpreted as primitive for the Osteichthyes by extrapolation of trends in actinopterygian and
sarcopterygian lineages. It is the most primitive known osteichthyan.
The Osteichthyes are considered to have arisen from a micromerically-scaled acanthodian or
acanthodian-like ancescor at the end of the Silurian period.
KEY WORDS:-palaeonisciforms - Cheirolepu - Osteichthyes - scales - locomotor improvemrnt
-
liulctloll.
CONTENTS
. . . . . . . . . . . . . . . . . .
Introduction
. . . . . . . . . . . . . . . .
General remarks
Classification . . . . . . . . . . . . . . . . .
Methodology . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . .
Primitive palaeonisciforms
The major affinities of Cheirolepis and the osteichthyans: previous work
The major affinities of Cheirolepis: present work
. . . . . .
Evolution within the genus Cheirolepis
. . . . . . . . .
. . . . . . . . . .
Characters of the stegotrachelids
Discussion: theearlyevolutionofthe Actinopterygii . . . . .
Features of osteichthyan diversification
. . . . . . . . . . . .
The primitive bony fishes
Discussion: adaptive radiation of the bony fish
. . . . . .
Affinities of the bony fishes
. . . . . . . . . . . .
. . . . . . . . . . . . . . . . . .
Conclusions
. . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . . . . . .
References
Abbreviations used in figures . . . . . . . . . . . . .
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46
D. M. PEARSON
INTRODUCTION
General remarks
Over the last ten years, a flood of new data has arrived bearing on the structure
and affinities of early osteichthyans (i.e. bony fishes). The structure of the
Devonian palaeonisciforms in particular has become much better known (Dunkle
& Schaeffer, 1973; Gardiner, 1973; Gardiner & Bartram, 1977) and it has become
increasingly clear that during the early Devonian period the osteichthyans were
undergoing a wide adaptive radiation. This paper is an attempt to relate what we
know of the structure of the Middle to Upper Devonian palaeonisciform Cheirolepis
(Pearson & Westoll, 1979) to that of other Devonian palaeonisciforms and thus to
clarify certain aspects of this radiation. This leads naturally to a consideration of
the broader relationships of the Osteichthyes.
Clessification
The classification adopted here reflects the traditional view that the Osteichthyes
are a natural group. Within the class, the Actinistia (coelacanths), Dipnoi and
Crossopterygii are considered to be more closely related to one another than they
are ro the Actinopterygii (Miles, 1975, 1977). The shared major character of two
dorsal fins in the first three groups points clearly to this conclusion (seealso Miles,
197 7 :3 10). The term Sarcopterygii coined by Romer (1955) to unite these three
groups is employed here, although it is slightly inappropriate in that a fleshy lobe
at the base of the paired fins seems to be a primitive feature of the bony fishes in
general.
The use of the taxon Teleostomi either as a synonym for Osteichthyes (Gross,
1962, 1969) or to embrace the Acanthodii and Osteichthyes (Moy-Thomas &
Miles, 197 1 ; Miles, 1975, 1977; Gardiner, 1973; Schaeffer, 1975) is rejected on the
grounds that the traditional use of the term has been to join the actinopterygians
and the crossopterygians (sensuluto, including the coelacanths) and to exclude the
acanthodians and dipnoans (e.g. Bridge, 1904; Goodrich, 1930). It is therefore
inherently ambiguous and ‘Osteichthyomorpha’ is used here to group together
the acanthodians and the bony fish.
While Cheirolepis is obviously a palaeonisciform, it is not a ‘typical’
representative of the order in the way of the members of such families as the
Palaeoniscidae, Elonichthyidae, Stegotrachelidae, Pygopteridae and many others
(Gardiner, 1963, 1967a). The vast assemblage of the chondrosteans is probably
best organized in a horizontal classification recognizing locomotory improvement
and jaw mechanics as the major criteria, but this is beyond the scope of the present
work.
The members of the family Cheirolepididae will be referred to as ‘the
cheirolepids’ throughout this work.
Superclass Osteichthyomorpha
Class Acanthodii
Class Osteichthyes
Subclass Actinopterygii
Superorder Chondrostei
Order Palaeonisciformes
PRIMITIVE BONY FISHES
37
Families Cheirolepididae, Tegeolepididae, S tegotrachelidae,
Osorioichthyidae, etc. (See Gardiner, 1967a, 1969).
Other actinopterygian taxa omitted.
Subclass Sarcopterygii
Infraclass Crossopterygii
Superorder Quadrostia
Order Osteolepidida
Order Rhizodontida
Order Onychodontida
Superorder Binostia
Order Holoptychiida
Order Actinistia (Coelacanthida)
Infraclass Dipnoi
Methodology
The methodology of the business of detecting phylogenetic affinity and erecting
phylogenies should include as its first tenet the economical explanation of the
observed evidence. Second and third tenets should be that subsequent stages in
any postulated phylogenetic series should be capable of functioning as organisms
and should be demonstrated to have possessed selective advantage over the prior
stage. Thus, increasing mechanical efficiency in any region of the musculo-skeletal
system of fishes will be advantageous because, other things being equal, it will free
more chemical energy for growth and reproduction (Alexander, 1967).
A primitive character for a group is a character, or its expression, which is
present in the group’s ancestral population. The recognition of truly primitive
characters is crucial in the interpretation of relationships. Wherever possible, the
interpretation of a character as primitive will be justified here by a consideration of
its role in the assemblage of characters which allowed that ancestral form to
function as an organism. To designate a character as primitive or advanced
without such a justification is empty.
PRIMITIVE PALAEONISCIFORMS
The major affinities of Cheirolepis and the osteichthyans:previouswork
The opinions of most of the authors writing on the affinities of Cheirolepis in the
nineteenth century have been reviewed by Traquair ( 1875). For the most part, they
are of historical interest only. Agassiz ( 1844-51, who erected the genus, considered
Cheirolepis to be an acanthodian transitional between other acanthodians and the
palaeonisciforms. Miller ( 186 1) doubted an acanthodian position for the genus
and discussed it in the context of such other genera as Osteolepis, Holoptychius,
Glyptolepis and Dipterus. 0ther contemporary authors considered Cheirolepis to be
an acanthodian, with varying degrees of doubt raised by the similarity of the headbone pattern to that of Palaeoniscum. Traquair (1875) established the genus as a
genuine, although early, palaeonisciform and to him this precluded any
relationship with the acanthodians. This view has dominated for a hundred years.
Following Traquair, the general tendency has been to view the micromeric
squamation as a convergence with that of the acanthodians. Watson (1925, 1935)
38
D. M . PEARSON
was especially emphatic in this direction, for he was very much concerned with the
establishment of cranial bone homologies within the Osteichthyes and he
considered a close relationship of Cheirolepis with the acanthodians incompatible
with its close relationships with the crossopterygians. Later authors, however
(Lehman, 1947, 1958, 1966; Lemaire, 1957;Jarvik, 1960, 1962, 1964, 19681, have
opined that Cheirolepis is an absolutely typical palaeonisciform, showing no more
resemblances to crossopterygians than do any other members of the order.
Concerning the relationships of the cheirolepids with other palaeonisciforms,
current opinion (Gardiner, 1967a; Schaeffer, 1973) denies that they gave rise to
any evolutionary descendants. Thus, Cheirolepis is seen as occupying a rather
isolated position : an early palaeonisciform, evolutionarily sterile, possessing
many primitive features but in its micromeric squamation and certain other
features, somewhat specialized also.
Evidence, meanwhile, continues to accumulate that the Osteichthyes is a natural
group (Jarvik, 1944a; Lehmann & Westoll, 1952; Denison, 1968b; Schaeffer,
1968; Gardiner, 1973; Andrews, 1977; Miles, 1977),but the precise composition
of the class and the relationships of the comprising groups are still matters for
debate (Bertmar, 1959; White, 1966; Jarvik, 1967; Bjerring, 1973; Miles, 1975,
1977; Wiley, 1979; Forey, 1980). Opinion seems to be hardening that the
actinopterygian- sarcopterygian dichotomy is an early and fundamental division
within the class.
Recent histological work on squamation (Gross, 1973)has interpreted as merely
superficial any resemblance between the scales of Cheirolepis and acanthodians.
Morphological studies of acanthodians (Miles, 1964, 1965, 1968, 1970, 1973a,b ;
Moy-Thomas 8c Miles, 197 1) have uncovered some apparently fundamental
resemblances in the neurocranial architecture to osteichthyans (especially the
actinopterygians)but the consensus from this area is that theacanthodians and the
osteichthyans show a phylogenetic relationship that is essentially sibling (MoyThomas & Miles, 1971; Miles, 1973b). This has been reinforced by new
information on the acanthodian dentition (Izlrvig, 1967, 1973)but the unsatisfactory knowledge of the acanthodians, especially the early ones, is reflected in the
extent to which it is still possible to defend a thesis of acanthodian relationship
with the elasmobranchiomorphs (Jarvik, 1977).
The major ajjnities of Cheirolepis :present work
I t is appropriate to start a consideration of the affinities of Cheirolepis with an
emphasis of its actinopterygian status. In the following diagnostic features
(Pearson & Westoll, 1979) i t is a typical palaeonisciform:
t 1 ) There is no exocranial joint along the fronto-parietal suture (Fig. 1).
( 2 ) The dermal skull includes triangular dermohyal and accessory opercular
bones (Fig. 6).
( 3 ) The dermal cheek unit consists of only five bones: preoperculum, maxilla,
quadratojugal, jugal and lachrymal (Fig. 6).
(4) There is a ring offour sclerotic bones.
( 5 ) The laterosensory canal pattern of the cheek involves a preopercular canal
which does not make any anastomosis with the infraorbital canal
postorbitally. In the snout region the supraorbital canal runs between the
incurrent and excurrent nostrils.
39
PRIMITIVE BONY FISHES
P. Pr
A Pr
/
L.Pr M P r
\
-
Exsc
10 mm
”
1
I rnm
I
10 mm
I
I
Figure I . Cheirolepis (after Pearson & Westoll). A, C. trailli, dorsal view of skull roof; B, C. canadensis,
dorsal view ofskull roof; C, C. trailli, scale; D, C. canadensis, scale.
(6) The dermal investment of the mandible consists of a large dentalosplenial
element plus an angular, prearticular, surangular and a row of coronoids.
( 7 ) The dentition comprises minute and small teeth only.
(8) The dermal pectoral girdle includes a small postcleithral bone lying
posterior to the cleithrum-supracleithrum articulation.
(9) There is only one dorsal fin.
(10) In the heterocercal tail there is a scale inversion and paired row of dorsal
caudal fulcra.
The overall morphology leaves no doubt as to the major affinities of the fish. It is
an indisputable palaeonisciform.
The following features of Cheirolepis (Pearson & Westoll, 1979) are not those of a
typical palaeonisciform. Their interpretation is given as appended letters and this
interpretation will be discussed in one or more of the various sections of this
paper.
A: primitive actinopterygiancharacter
0 : primitive osteichthyan character
Q: primitive osteichthyomorph character
G : primitive gnathostome character
40
D. M. PEARSON
( 1 ) The dermal mosaic rostrally: AOQ (Fig. 4A).
( 2 ) The presence of preorbital and supraorbital bones: A 0 (Figs 4A, 6A: ‘Pro’,
‘Spo’).
( 3 ) The absence of anamestic suborbitals between preoperculum and the bones
of the posterior circumorbital region (Figs 1,4A, 6A).
(4) The long jaws: A 0 (Fig. 6A).
(5) The presence of a pineal plate (=posterior postrostral): AOQG (Fig. 1 ) .
(6) The presence of a central cranial laterosensory canal (C. trailli only): AOQG
(Fig. 1A: ‘Cen.c’).
1 7 ) The seeming absence (C. trailli only) of cross commissures between the
medial ends of the ethmoid and occipital laterosensory canals: AOQG.
(8) The parietals as long as the frontals: A 0 (Fig. 1).
19) Large lateral gulars, approximately four times the length of the median
gular: A 0 (Fig. 7A).
( 10) A very narrow, blade-like parasphenoid devoid of even rudimentary
ascending processes: A 0 (Fig. 8A).
( 1 1 ) The micromeric dermal investment of the anterior palate: AOQ.
( 121 The presence of an interclavicle: AO.
( 13) The apparently long pectoral endogirdle: AOQG.
I14) The long lobate bases of the pectoral fins: AO.
(15) The micromeric squamation: AOQG.
(16) The absence of a peg-and-socket apparatus linking the adjacent scales in
each scale-row: AOQ.
( 1 7 ) The presence of a ventrolateral scale-row inversion: AOQ.
( 1 8 ) The caudal axial lobe: AOQG.
(19) The elongate body: AO.
I t is likely that some of these characters are expressions of the same general
morphogenetic system and therefore should be considered together (e.g. a
general micromery linking 1, 2, 5, 1 1 , 15 and 16).
Evolution within the genus Cheirolepis
In the following characters (Pearson & Westoll, 19791, the Upper Devonian
Cheirolepis canadensis is more advanced than the Middle Devonian C. trailli:
i 1 ) The reduction of the posterior postrostral element and the consequent
meeting of right and left frontal bones anterior to the pineal foramen
(Fig. 1B).
(2) The longitudinally-striate dermal cheek bone ornament, as opposed to the
pitted pattern seen in C. trialli.
( 3 ) The probable presence of a full, continuous occipital commissure (Fig. 1B).
(4) The absence of a central cranial laterosensory canal (Fig. 1B).
( 5 ) The shorter spines on the scales (Fig. lC, D).
Characters 3, 4 and 5 are of doubtful significance because of either less than
certain knowledge of the range of variation in Cheirolepis, or an inadequate
knowledge of the primitive state.
Lemaire (1957) detected a more vertical suspensorium in C. canadensis than in
C. trailli but this is by no means obvious and there is considerable variation in the
PRIMITIVE BONY FISHES
41
morphology of the maxilla in both species, so the point must remain dubious.
The two characters in which C. canadensis appears to be more primitive than
C. trailli (micromeric postrostrum, more scale-rows per body somite) are
interpreted here as consequences of its larger size (see below).
Cheirolepis canadensis possesses no features preventing its derivation from the
earlier (by about 15 My) C. trailli. Some of the changes it shows from the latter
parallel changes which have occurred along the line leading from the cheirolepid
to the stegotrachelid (or ‘typical’)level of palaeonisciform locomotor organization. The ornament rearrangement is an example here; this was possibly in the
interests of promoting laminar flow around the head.
The larger size of C. canademis (up to c. 550 mm, as opposed to the c. 350 mm
maximum of C. trailli, Pearson & Westoll, 1979)appears to have led to a number
of body changes, e.g. the relative increase in pelvic fin area to counter the higher
rolling momentum, and the broader and flatter anterior region of the head. This
last phenomenon occurs in Polypterus today, where the larger species have a more
depressed cranium than the smaller ones (Lewis, 1974:fig. 3A). This may be an
adaptation to increase the ventral surface area of the head in order to gain the
extra lift necessitated by any net bodyweight increase. In Cheirolepis, this process
of relative broadening and flattening may have led to the splitting of the
...
A
r.ophtha1rnicu-s
suoerficialis
r.oticus and
r.derrnosphenoticus
---
n.glossopharyngeus
II[
r.vagus lateralis
0000
L
Figure 2. Possible steps in the evolution of the laterosensory canal system of the head in bony fishes.
Enclosed symbols indicate sensory canals; open symbols indicate pit-lines. A, Hypothetical pregnathostome condition, with independently innervated separate canals; B, ancestral gnathostome
condition, also seen in primitive placoderms and primitive osteichthyans, with canals joined up
longitudinally by primary tubule anastomosis in the temporal region; C, typical palaeonisciform
and early sarcopterygian condition, with the occipital commissure; D, condition exemplified by
advanced actinopterygians and typical sarcopterygians, with anastomosis of supraorbital and
infiaorbital canals in the postorbital region.
-12
D. M . PEARSON
originally single anterior postrostral bone of C.trailli into the three elements
lying across the snout of C. canademis (Fig. IA, B).
If the micromeric squamation is indeed related to the locomotory mode, as
seems likely, then perhaps some hydrodynamic or other mechanical factor
limited the rostro-caudal length of the cheirolepid scale to c. 0.8 mm. For
example, it would seem that too long a scale would inhibit high-amplitude
undulations on the concave side of the body curve (see also below, p. 44).In this
case, the greater size of C. canadensis would lead to the observed higher number of
scale-rows insertable into a single body somite length, from the c. 5 of C. trailli to
c. 7 .
A full occipital commissure is probably more advanced than a medially
incomplete one because the history of the laterosensory canals in the
actinoptelygian (and sarcopterygian) exocranium is one of anastomosis. The
familiar eventual junction of the supraorbital and infraorbital canals behind the
eye, which has occurred quite independently in actinopterygians,
crossopterygians and dipnoans, is a case in point. Extrapolation of this process
back i n time leads us to a picture of rather separate canals on the heads of
primitive bony fish, perhaps with each canal innervated by a different ramus of
either the anterior or posterior lateral-line nerve of the head (Fig. 2). The central
canal is recorded only in C. trailli among the actinopterygians, but it is also found
in ,24~galzchthys among the sarcopterygians (Bjerring, 1972). Its presence in
placc.,”rms (Stensio, 1963, ‘ifc.b’) may indicate that it is common to primitive
gnathostornes (Fig. 2B). The overall evolutionary trend suggests the transformation of a primitively radially-symmetrical pattern of canals (at perhaps the
agnathan level) to a bilaterally-symmetrical pattern with canals joined up by
anastomoses and cross-commissures rostrally and occipitally. This would imply a
contemporary change in habit from a sessile to an active mode of life.
Characters of the stegotrachelids
The stegotrachelids are generally considered to be the most generalized of the
Devonian palaeonisciforms and the ancestors of most subsequent
actinopterygians (Gardiner, 1970, cf. Gardiner, 1967a; Schaeffer, 1973).
Thanks to the work of Rayner (1951, Kentuckia), Jessen (1968, 1972a,
Moythomasia), Gardiner ( 1963, Stegotrachelus ; 1973, Moythomasia, Mimia) and
Bartrarn (Gardiner & Bartram, 1977, Moythomasia, Mimia), the predominantly
Devonian stegotrachelids are now known in considerable detail. They differ from
the cheirolepids in lacking the following features:
( 1 ) The nasal/rostral mosaic (Figs 4B, 6B-D).
(2) A separate ossification associated with the pineal foramen (Fig. 3A, B).
( 3 ) An interclavicle.
( 4 ) The supraorbital and preorbital bones (Fig. 6).
I n addition, the stegotrachelids show a number of characters different to their
expression in the cheirolepids:
(5) The body, fins, pectoral endoskeleton, jaws and headbones are relatively
shorter.
(6) The parasphenoid has the beginnings of ascending processes (Fig. 8B, C ) .
( 7 ) The lateral gulars are only about twice the length of the median gular
(Fig. 7B).
43
PRIMITIVE BONY FISHES
n
D
Figure 3. Palaeonisciform skull roofs, showing the progressive reduction of the parietal bones
(shaded)and the extension of the fronds. Not to scale. A, Moythomasia nitida (afterJessen, 1968, with
the spiracular opening re-positioned according to his Plates); B, Kentuckin deani (after Rayner); C,
Pteronisculus stensioei (after Nielsen); D, Boreosomus piueteaui (after Nielsen) ; E, Coccocephalichthys wildi
(atter Watson); F, Birgeriagroenlandica (after Nielsen).
44
D. M. PEARSON
( 8 ) The pectoral fin endoskeleton has some form of metapterygial element
developed in the posterior region of the row of basal pterygiophores.
(9) The squamation consists of peg-and-socketed scales with about two scalerows to each body somite (Fig. 5E).
(10) Anamestic suborbital bones are present at the anterior end of the
preoperculum (Fig. 6B-D).
I t will be argued below that these changes represent adaptations in the
interests of craniomechanical or locomotory improvement and constitute early
steps along evolutionary paths which continue beyond the stegotrachelids in
more progressive palaeonisciforms.
Discussion: the ear4 evolution ofthe Actinopterygii
Characters in the above list having to do with locomotion will be considerd
first. Pearson 8c Westoll (1979) have noted that the small scales, fin assemblage
and elongate body form of Cheirolepis are probably related to a ‘selachian’
method of swimming where waves of contraction pass back along the body
gaining amplitude as the body tapers posteriorly. In modern fish, at least, there is
an inverse correlation between scale-size and swimming-wave amplitude (Aleev,
1969). One rationale for small scales is that they result in a high number of
interscale shear-lines in the integument. This shear is produced by the
interaction of the simultaneous compression and tension forces generated by
myotomal action and which appear at the surface of the animal. As a result of the
large number of small scales, the skin is capable of great and uniformly-spread
deformation, so allowing the high amplitude undulations of this mode of
locomotion.
From an examination of the ‘typically’ large-scaled palaeonisciforms
(~lfoythornasia,Jessen, 1968: pl. 14, text-fig. 1 ; Pygopterus, Aldinger, 1937 : figs
37,42) it seems that there are generally two scale-rows per somite”. In more
advanced and living actinopterygians there has been a doubling of the scale size
relative to the somite and thus we see usually only one row per somite
!Aurlralosomus, Nielsen, 1949; Polypterus, Pearson, 198 1 ; Leuciscus, Goodrich,
1909:fig. 193). This increase in scale size while passing to the ‘subholostean’ level
has been accompanied by a number of other locomotor refinements in the areas
of fin, tail and scale morphologies. Alexander (1969), furthermore, has noted a
change in the myotomal architecture from an elasmobranch-like shape in the
most primitive living actinopterygians (e.g. Erpetoichthys, Acipenser) to a more
complex ‘typically teleostean’ type.
The general increase in scale size from the two rows per somite in typical
palaeonisciforms to the single row of extensively overlapping cycloid scales of
teleosts must have had the effect of reducing the passive flexibility of the body (by
stif‘fening the skin and preventing concave body waves of high amplitude) and it
was probably related to the evolution of a swimming pattern where the
amplitude of the locomotory waves in the trunk was considerably reduced while
the frequency of the waves was increased (Aleev, 1969). This process was assisted
by the lateral compression of the body, which increased the lateral resistance to
the water. One of the benefits of lateral compression (Liem, 1977: 198) is that it
reduces yaw. In general, these locomotory improvements occurring between
Nielsen(1942.2551records threeforPferontscultubut hishgureshgs50,57)suggestonlytwo
PRIMITIVE BONY FISHES
45
typical palaeonisciforms and teleosts are in the same direction as those which
have occurred in the typical palaeonisciforms themselves over the cheirolepids.
Moythornasia has larger scales than Cheirolepis and is more laterally compressed
(Fig.4).
Figure 4. Anterior views of the reconstructed head of A, Chezroolepis trailli (after Pearson 8c Westoll); B,
h’oylhoirinsin nitzdu (after Jessen, 1968, with the spiracular opening re-positioned according to hi6
Plates). N o t to scale.
Another stegotrachelid adaptation to decrease the yaw which seems to have
afflicted Cheirolepis (Pearson & Westoll, 1979) is a shortening of the body. Yaw is a
passive reaction of the front part of the body to the locomotory waves of the rear
part (‘the tail wagging the fish’). Therefore, any reduction of body-length will
reduce the amplitude of the transverse sweeps made by the body at each end of
the animal. Reduction of yaw results in not only more accurate directional
swimming but also the expenditure of a smaller amount of energy while
swimming (Alexander, 1967 and will thus be advantageous.
While reducing the amplitude of the trunk locomotory movements, the
actinopterygians also show a progressive functional separation of tail from body
in their mainstream evolution. The first stage in this separation (Watson, 1925)
was the development of the caudal scale inversion and the dorsal fulcra, both of
which are present in Cheirolepis. The caudal inversion (Patterson, 1968)produces
an exoskeletal line or zone of weakness at the tail base of palaeonisciforms which
must have acted as a hinge for the tail on the body. Caudal fulcra, by crossing
several somites, restrict the degree of lateral flexure of the caudal vertebrae, i.e.
stiffen the tail dorsally and help it to act as a single blade. Both dorsal fulcra and
the caudal scale inversion are found only in actinopterygians and obviously are
functionally related characters. Teleosts, of course, have largely abandoned
undulatory for caudal swimming (Gosline, 197 1) and this locomotory mode has
an advantage of further reducing yaw by damping lateral undulations of the
D. M . PEARSON
Hi
body (Gray, 1933b; Nursall, 1962). It seems, therefore, that yaw has been
reduced progressively during much of actinopterygian evolutionary history.
The typical palaeonisciform tail lacks an axial lobe, although some form of
axial lobe is retained in ParamblyPterus (Blot, 19661, Cosmolepis and Palaeoniscum
(Watson, 1925)and Belichthys (Hutchinson, 1975). In its typical manifestation the
tail, devoid of an axial lobe, represents an early stage in the progressive
abbreviation of the body lobe of the actinopterygian caudal fin which eventually
resulted in the homocercal tail of teleosts.
in the light of all this, Cheirolepis may be seen as a logical forerunner of the
typical palaeonisciforrn level of locomotory evolution, which is itself the stage
antecedent to the modern forms. Another micromerically-scaled Devonian
palaeonisciform is Tegeolepis, with five scale-rows per somite (Dunkle 8c Schaeffer,
1973).This genus is specialized in its long cranium and the thin scales suggest the
result of a process of reduction (Gardiner, 1963). This in turn poses the
possibility of this process being accompanied by a secondary return to
micromery. Cheirolepid scales, on the other hand, are as thick as they are long
and high and no such reductive or secondary processes seem to have occurred.
The Carboniferous Turraszus (Moy-Thomas, 1934; Jessen, 1973a)has three scalerows per somite in the posterior region of the body and has lost all more anterior
scales. This, together with its continuous median fin, allowed an anguillid mode
of locomotion (Westoll, 1944; Moy-Thomas & Miles, 1971) which is an
exaggerated version of the selachian type and from which it is presumably
derived (Gray, 1933a; Lighthill, 1960). The relationship of Tarrasius are obscure
(Schaeffer, 1973) but it is generally thought of as secondarily derived from typical
palaeonisciforms (perhaps the holurids), principally on the grounds of its
advanced dermal skull, fin-rays and fin-assemblage. In contrast to Tarrasius,
Cheirolepis shows no obviously advanced characters along with its micromery ; it
},.<is. A completely
.
scaled, fusiform body and not the cylindrical trunk of the typical
;tiiguillid-mode swimmer. Again, therefore, this indirect and circumstantial
cvidciice reinforces the conclusion that the cheirolepids are primitively
niicromeric.
Direct evidence on the scale size in the earliest actinopterygians is ambiguous.
Isolated ‘actinopterygian’ scales have been reported from the Lower Devonian
(Schultze, 1968, 1977)and the Upper Silurian (Gross, 1968, 1969, 197 l b ; Janvier,
1978). The latter are less impressively actinopterygian than the former and
probably relate more to ancestral osteichthyan populations than to ancestral
actinopterygians and they are considered below. The two Lower Devonian
genera have a single-layered ganoine and a peg-and-socket apparatus. One
genus, Ligululepis (Fig. 5A, B), has tall and narrow scales of c. 0.8 x up to 3 mm,
while the Dialipina scales are squarer and, at c. 2 x 2 mm, about a normal
palaeonisciform scale size. Vertebral evidence, however, is necessary before any
information on scale-row to somite relationships can emerge. The occurrence of
elongation and peg-and-socket articulations indicates the very early
development of locomotory improvement in the actinopterygians. The argument
has been developed above that in neither the scale structure nor arrangement
does the micromery of Cheirolepis seem to be secondary. Reconciliation of these
lines of evidence is possible if the genus is seen as a long-lived survivor from the
early part of the Lower Devonian. This argument has already led Pearson 8c
Westoll (1979:394) to suppose that the fish is a generally archaic form, owing its
continued existence to a competition-free ecosystem. Given the nature of both
,
PRIMITIVE BONY FISHES
47
E
Figure 5. Representative scales of early osteichthyans (to the same scale). A, Lzgulalepis toombsi, inner
view; B , Ligulalepis toombsi, outer view; C , Lophosteus superbus, outer view; D , Lophosteus superbus, inner
view; E , Moythomia nitida, outer view. A and B after Schultze, C and D after Gross, E after Jessen.
the geographical radiation and fossilization processes, anachronisms are
common in the fossil record. Late-lived typical palaeonisciforms (Triassic) are
seen in Pteronisculus, a genus whose overall organization seems typical of other
genera from the Permian or even the Carboniferous. The earliest stegotrachelid,
Stegotruchelus from the Middle Old Red Sandstone of the Shetland Islands, in
such features as the short parietals and the loss of both dermohyal and accessory
opercular bones, is the most advanced form of the entire family (Gardiner, 1963;
Fig. 6D). Later genera (Moythomusia: U. Devonian, Kentuckia: L. Carboniferous)
retain a more primitive exocranium (Figs 3A, B, 4B, 6B-D).
The stegotrachelid pectoral fins have a narrower base than those of the
cheirolepids and the endoskeleton is more concentrated (Jessen, 1968; Fig. 91,
suggesting that they were more mobile. This would indicate further
improvements in locomotor control.
Apart from the scales, perhaps the most striking skeletal difference between
Cheirolepis and the stegotrachelids concerns the endoskeleton of the pectoral fin
and girdle. The fin endoskeleton of Moythomusia (Jessen, 1968:fig. 8 ; Fig. 9) is
derivable from the condition in C. trailli by a process of base constriction, a
slimming and elongation of the basal pterygiophores and a reinforcement of the
first and last elements in the row. All these changes can be related to improving
the manoeuvrability while retaining the stiffness of the fin.
The long endogirdle of C. trailli (Pearson 8c Westoll, 1979:figs 12, 14),
articulating as it appears to do with the inner surface of not only the cleithrum
18
D. M . PEARSON
but the 'clavicle also, has shortened considerably in the stegotrachelids
(Mo~'thomusiu).The attachment is now limited to the cleithrum. Our inadequate
knowledge of the precise structure of the Cheirolepis endogirdle limits further
discussion but it is reasonable to suppose that this shortening is, at least partially,
one aspect of a general shortening of the body which is reflected in such other
areas as fin-bases, jaws and tail. A pectoral endogirdle extending far anteriorly
occurs in primitive placoderms (Stensio, 1959) and probably in primitive
acanthodians also (Watson, 1937; Miles, 1973a1, and so it is probably the
primitive gnathostome condition.
An interclavicle seems to be a primitive osteichthyan possession because one is
present in Cheirolepis and some other primitive actinopterygians (Westoll, 1944;
Patterson, 1977), primitive Dipnoi (Denison, 1968a, b) and crossopterygians
(Jarvik, 1944a, 1972).
Turning now to cranial morphology, the anamestic and canal bones of the
rostral area of Cheirolepis are absent in the stegotrachelids, whose premaxillae
contact the sole (anterior) postrostral element in the typical palaeonisciform
manner (Gardiner, 1963). This appears to be related to the shorter jaw requiring
less rostra1 elevation and deformation when widely open and to a stabilization of
the anterior ramus of the maxilla by a firm suture with the premaxilla. This is
presumably in the interest of a stronger bite. The general increase in the size of the
orbit in the stegotrachelids over the cheirolepids (Fig. 6) has also contributed to
the loss of the rostral mosaic (and involved the loss of the preorbital and
supraorbital bones, both of which are present in cheirolepids and
sarcop terygians).
The solid and unfragmented nature of the postorbital region of the dermal skull
of Cheirolepis stems from the doubtless very extensive ventral otic fissure and the
resultant mechanically weak neurocranium (Pearson & Westoll, 1979:386). The
parasphenoid of the cheirolepids is nossopterygian-like in its lack of ascending
processes (Fig. 8A, E) so it is likely that the otic fissure was more anterior in
position and extended further dorsally than in the stegotrachelids. In these, the
smaller postorbito-dermosphenotic and fragmented preoperculum are reflections
of the greater strength of the basisphenoid, allowing a less extensive dermal
bracing and the 'loosening-up' of the cheek. With a more movable palatoquadrate, the versatility of the jaws is increased.
The early stages of the continuous sequence of change which marks the
actinopterygian jaw and cheek mechanism are well known (Schaeffer 8c Rosen,
1961; Wenz, 1962; Gardiner, 1967b, 1973). They involve an increase in palatoquadrate mobility as a result of a gradually less intimate palatobasal articulation
and a fragmentation of the dermal skull in the postorbital region (the bones
involved are the postorbito-dermosphenotic, the preoperculum and the jugal). A
shortening of the jaws lightens the loading arm of the mandible and thus increases
the power of the bite. The process results in the familiar apparent anterior
migration of the articulation so that the posterior ramus of the preoperculum
comes to lie caudal, rather than dorsal, to the maxilla (Fig. 6). Again, the condition
in Cheirolepis forms a logical earlier stage to that seen in stegotrachelids. It is likely,
therefore, that in its long jaws and oblique suspensorium Cheirolepis is primitive.
The cheirolepid gular architecture (Fig. 7A) is clearly the most primitive known
among actinopterygians since it is not only the condition predicted by extrapolation of the subsequent trend in actinopterygian gular evolution (enlarging median
gular and diminishing lateral gulars, Fig. 7A-D) but also conforms to the pattern
PRIMITIVE BONY FISHES
D
Figure 6. Lateral views of palaeonisciform exocrania. Not to scale. A, Cheirolepis trailli (after Pearson
& Westoll); B, M o y t h o m i a nitida (after Jessen, 1968, with the spiracular opening re-positioned
according to his Plates); C, Kentuckia deani (after Rayner); D, Stegotrachelus ,finlayi (after Gardiner,
1963, but altered in that the spiracular opening has been restored to its probably correct position);
E, Palaeoniscumfreiesl~beni(afterWestoll in Aldinger); F, Pteronisculus stensioei (after Nielsen).
49
Figure 7 , Gular region 01. pl-iniitivc osteictithyans. Not to scale. A, Chezrokpis lradli (after Pearson Be Westoll); B, Moylhomnzn nilzdn (after Jessen); C,
Pteronisculus magna (after Nielsen);D, Birgerza groenlandica (af'ter Nielsen); E, Osteolepis macrolepzdotus (afterJarvik); F, Porolepis brevzs (afterJarvik).
i;
P
PRIMITIVE BONY FISHES
51
of small median and large laterals displayed by the early sarcopterygians (Fig. 7E,
F; see also below). The direction of gular evolution in chondrosteans is related to
the increasing lateral compression and the elimination of the flat underside of the
head and body which were part of the sequence of locomotor improvement
occurring in the palaeonisciforms.
The structure of the cheirolepid palatoquadrate calls for some comment. The
peg and hole nature of the palatobasal articulation (Pearson & Westoll, 1979:fig.
8 ) was carried forward unchanged into the stegotrachelids (Rayner, 1951;
Gardiner, 1973) and beyond (Pteronisculus cicatrosus, Lehman, 1952) but in more
advanced palaeonisciforms a less restrictive articulation occurs, related to the
increased mobility of the whole palatoquadrate-dermal cheek assembly.
The anterior entopterygoid series of bones may be the remains of an originally
micromeric dermal investment of the palate (Schaeffer, 1975; cf. Gross, 1971a)
covering most of the buccal surface of the upper and lowerjaws. If this is so, then
these bones represent the unspecialized condition from which palatines,
coronoids, pterygoids and the other dermal bones of the oral cavity have been
derived. They are also the serial homologues of the toothplates borne on the
branchial arches more posteriorly. In a second class lever system like the jaws of
the early palaeonisciforms, the greatest out-forces are developed close to the
fulcrum (as in a pair of nutcrackers). This seems to have been a major factor
leading to the development of, initially, a dermal element in the posterior region
of the upper jaw, the posterior (main) entopterygoid bone (= ectopterygoid,
Nielsen, 1942). Selective pressure to extend or duplicate this anteriorly was
apparently less intense and resulted in the dermal investment of the autopalatine
region of the palatoquadrate retaining its primitive micromeric organization
longer. Presumably, on the ‘mirror-image’principle which seems to operate in the
upper and lower jaws of primitive gnathostomes (Watson, 1925; Romer,
1970:240), we could expect the occurrence of a number of small toothplates
ventral to the coronoids on the buccal surface of the intermandibular region of
Cheirolepis, but none have been seen (but note Pteronisculus, Nielsen, 1942:fig. 38,
(0s’).
The Middle Devonian appearance of the stegotrachelids at present precludes
their derivation from the C.trailli populations of those times but there do not seem
to be any morphological barriers to such a relationship. Some earlier
palaeonisciform at the cheirolepid level of organization is indicated for this role.
The large size of the pineal foramen in the stegotrachelids is quite possibly an
artificial condition resulting from the further reduction of the cheirolepid
posterior postrostral element to either a ring of very small, easily lost ossicles (such
as occur in Eusthenopteron, Jarvik, 1944b) or a fibrous sheet occupying the bony
foramen and bearing the smaller true foramen. Even from the short period of
known cheirolepid history, it is quite evident that this region of the skull roof was
in a state of change involving the reduction in size of both the pineal foramen and
its surrounding bone. Apart from the cheirolepids and the stegotrachelids,
there are other palaeonisciforms bearing a pineal foramen (e.g. Gyrolepidotus,
Oxypteriscus, Ganolepis, Ministrella and Palaeobergia, Kazantseva, 19681, but it is
absent in the majority of forms. The final manifestation of the foramen is in the
form of a ‘macula’ as in Pteronisculus (Lehman, 1952:fig. 2 1) and the haplolepids
(Westoll, 1944). The retention of the pineal foramen cannot be a specialized
character preventing the stegotrachelids being ancestral to later palaeonisciforms
(Gardiner, 1967a).
il
D. M . PEARSON
FEATURES OF OSTEICHTHYAN DIVERSIFICATION
Theprimitive bony fishes
The osteichthyan ancestral morphotype which emerges in the course of the
present work is as follows:
Elongate-fusiform fish, operculate, with a micromeric squamation which lacks
both the enameloid and cosmine layers. Peg-and-socket apparatus also absent.
Scale-rows with a ventrolateral inversion along the line on each side of the body
joining the pectoral and pelvic fin bases. Fin complement of paired pectorals and
pelvics, with anterior and posterior dorsals, an anal and a heterocercal caudal
devoid of an epichordal lobe but with a small axial lobe. All precaudal fins with
long muscular bases and all fin webs stiffened by lepidotrichia. Cranial
exoskeleton macro-amphimeric, i.e. with large bones present in the flat, immobile
regions of the head and in those areas calling for strength; smaller bone elements
associated with regions of mobility. Parietals longer than frontals. Nasal in the
form of a series of bones bearing the supraorbital canal. A pineal orifice present in
a discrete bone between or in front of the frontals. Jaws long, suspensorium
oblique.
Dermal pectoral girdle as a chain of bones on each side of the body, linking the
single ventral interclavicle to the skull roof. Parasphenoid narrow and short,
bearing a foramen hypophyseos and lacking any ascending processes, its posterior
border marked by the extensive ventral otic-sphenethmoid fissure which is
akinetic and filled with cartilage. Dentition of small and minute teeth borne on the
dermal bones of the jaws and the toothplates of the oral surface of the palate,
intermandibular region and branchial arch elements.
Discussion: adaptive radiation of the bony fish
Characters of ancestral bony fish additional to those in the above list may be
found in Schaef'fer (19681, Moy-Thomas & Miles (1971)and Gardiner (1973).The
discussion, as throughout this paper, will be restricted to those characters whose
expression is known, or is reasonably inferrable, in Cheirolepis. Many of these
characters are familiar and will need little comment. The parasphenoid, for
example, is now known to be short (i.e. does not extend posteriorly beneath the
otic and occipital regions of the neurocranium) and without any ascending
processes in all the primitive members of the major groups of Osteichthyes (Fig.
8A, E, G ; Westoll, 1949; Lehmann & Westoll, 1952; Jarvik, 1954; Denison,
1968a, b; Gardiner, 1973; Pearson & Westoll, 1979).Thevery short parasphenoid
of holoptychiids (Fig. 8F; Jarvik, 1972) is the result not only of the abbreviated
snout directly but also of the wide degree of kinesis allowed by the endocranial
joint, perhaps in some way to compensate for this shortness of the anterior
division of the head (Thornson, 197 1).
All the early members of each major group of osteichthyans possess an elongate
body, although this was subsequently shortened in some. An elongate-fusiform
body shape was probably related to the ancestral swimming mode, which is
envisaged here as requiring a supple, small-scaled body to allow the propagation
of large-amplitude locomotory waves.
Direct evidence as to the scale-size in ancestral bony fishes is once again limited
to fragmentary material from animals of debatable affinities. Gross ( 1968, 1969,
197 lb) has described ornamented spines, small teeth and scales of less than 1 mm
PRIMITIVE BONY FISHES
53
Figure 8 . Outlines of the parasphenoid of various osteichthyans. Not to scale. A, Cheirolepis trailli
(after Pearson & Westoll); B, Mimia toombsi (after Gardiner & Bartram); C, Moythomasia durgaringa
(after Gardiner & Bartram); D, Pteronisculus m g n a (after Nielsen); E, Eusthenopteron foordi (after
Jarvik); F, Porolepis breuis (afterJarvik); G , Uranolophus wyorningensis (after Denison).
rostrocaudal length (Fig. 5 C , D)from the Upper Silurian (Ludlovian)of the Baltic
(see also Mark-Kurik, 1969). He tentatively suggested osteichthyan (more
especially actinopterygian) relationships for these genera (Lophosteus, Andreolepis).
Janvier ( 1978) agrees and concludes that Andreolepis most resembles Cheirolepis of
known genera.
As before, we must await more extensive material before any question of relative
scale size can be settled. It is becoming more apparent, however, that Cheirolepis
possesses points of histological and morphological resemblance with these early
0 steichthyans.
The sarcopterygians possess large scales of only one row per somite (Osteolepis:
Jarvik, 1948 :fig. 26; Andrews 8c Westoll, 1970b :fig. 5; Eusthenopteron: Andrews,
1973:fig. 1A; Andrews 8e Westoll, 1970a:fig. 23) and this was probably so from
the group’s inception (Porolepis: Orvig, 1957). The known scale history of
sarcopterygians parallels that of actinopterygians to a marked degree (Andrews,
1973).An apparently originally rhombic scale, with a peg-and-socket articulation
linking it to its two neighbours in the scale-row, lost the articulation, became
cycloid and lost the enameloid layer in actinopterygians and at least twice independently within the sarcopterygians. The suggested absence of an enameloid
layer in the scales of the first osteichthyans (Schultze, 197 7) is supported by the very
different nature of this region in the actinopterygiansand the sarcopterygians. In
the former group it takes the form of an uninterrupted ‘ganoine’ deposited on all
the exposed surface of the scale, whether this be dentine in the first instance or the
previous ganoine layer subsequently. Thus the enameloid, as is well known, builds
up like the skins of an onion and becomes thicker with age. In the sarcopterygians,
however, the enameloid layer is very thin and overlies a thick supraspongiosa layer
comprising the unique tissue cosmine. In the coelacanths cosmine is absent. It is
il
D. M. PEARSON
essentially a thick dentine extensively penetrated by tubules of the pore-canal
system which go on to pierce the enameloid and open on the scale surface. A
cyclical history of initial deposition and subsequent absorption to allow growth
further characterizes the cosmine of osteolepids and dipnoans (Westoll, 1936;
Izlrvig, 1969; Thomson, 1975, 1976b, 1977). The lack of the enameloid layer in
Andreolepis and Lophosteus (Gross, 1968, 1969) and its apparent beginnings in
Ligulalepis and Dialipina (Schultze, 1968, 1977) also lend some support to its
independent acquisition by actinopterygians and sarcopterygians.
True cosmine (Miles, 1977 : 311) is restricted to dipnoans and ‘rhipidistians’. Its
close physical relationship with the laterosensory system presumably indicates a
functional relationship also. Specifically, its adaptation towards the refinement of
an electrical exteroceptive capability has been mooted (Thomson, 197 7). If
correct, this would imply a turbid-water environment for early sarcopterygians,
since in existing fishes such a sensory modality appears to have been developed in
response to the special problems offered by this environment (e.g. in the African
Lakes, the mormyrids and malapterurids). The small eyes of nossopterygians
and lungfish when compared to the actinopterygians are well known and small
eyes are another common feature of modern turbid-water dwellers. The loss of
cosmine by the coelacanths (Miles, 1977:312) is therefore possibly related to a
colonization of clearer waters, where an electroceptive capability would appear
to be unnecessary on account of the greater range of the eye. In general, the eye
appears to be relatively larger in coelacanths than in other sarcopterygians.
In those early sarcopterygians and palaeonisciforms possessing rhomboid
scales, the squamation is likely to have had the important locomotory
function of maintaining the transverse plane of the swimming undulations by
preventing axial torsion of the body (Gutmann, 1975, 1977; Pearson, 1981).The
original rationale for scale-rows at c. 4 5 O to the longitudinal axis of the fish was
doubtless to allow shear between them during locomotion (Alexander, in litt.) but
this configuration is also optimal for the prevention of torsion. Exploitation of the
scale-row as a strut to brace the body-wall in this role involved an increase in the
mechanical strength, i.e. size, of each scale and the development of the peg-andsocket apparatus.
By interrupting shear-lines, peg-and-socket articulations reduce the overall
flexibility of the skin. The articulation, therefore, seems to be an adaptation at
least partially developed in a functional relationship to the type of swimming
which involved undulations of lower amplitude than in the ‘selachian’ mode.
The same is true for an increase in scale-size along either axis (rostrocaudal,
dorsoventral): they all diminish the number of shear lines available in the skin.
I t is possible, therefore, that we have to think of the osteichthyan peg-and-socket
articulation being produced a number of times (Schultze, 19771, together with an
elongated or enlarged scale, since both modifications appear to have developed
at least partially towards the same end. Having already noted the parallel
evolution in the scales of the various osteichthyan lineages, the likelihood of a
further parallelism in the history of the squamation seems reasonable.
A set of cycloid scales, as noted above, by virtue of their extensive overlap
relationships is related to a locomotory mode of even lower undulation
amplitude than in the typical palaeonisciforms (the subcarangiform mode,
Lindsey, 1978). The infrequent swimming habits of sarcopterygians (Thomson,
1969; Andrews & Westoll, 1970a, b) obviated a flexible body early in the group’s
history and led to the early loss of the micromeric squamation, the development
PRIMITIVE BONY FISHES
55
of a rhombic scale-form with a peg-and-socket apparatus and then their loss as
the cycloid squamation originated. In the actinopterygians, at a later date, the
fibrous dermis and vertebral ‘zygapophyses’ eventually took over the torsionpreventing functions of the squamation with a better weight economy as the
locomotory undulations became flatter. Thus in both actinopterygians and
sarcopterygians the peg-and-socketed rhomboid squamation was eventually
superseded by an overlapping cycloid one.
A ventrolateral scale inversion in the abdominal region is found in at least one
acanthodian (Westoll, 1958), ‘rhipidistians’ (Jarvik, 1948) and primitive
actinopterygians (e.g. Cheirolepis ; Moythomasia Jessen, 1968, 1972a; Indaqinilepis,
Schultze, 1970; Acropholis, Aldinger, 1937 :p1.5; the haplolepids, Westoll, 1944).
Its presence is probably associated with a primitively flat venter.
The most economical interpretation of the endoskeleton of the pectoral fins in
bony fishes, and its evolution, involves an original series of basal pterygiophores
running anteroposteriorly and, with the associated musculature, forming a fleshy
lobe along the base of the fin. A priori, a longitudinal row of basal
pterygiophores must be presumed to be more primitive than a row arranged
down the fin axis, since it approaches a simple metameric condition. Such an
arrangement also provides the fin with a long, stable base which enabled it to act
as a stabilizer, an important contribution to locomotor control. In
sarcopterygians this basal series appears to have been rather rapidly converted
into the axis of the ‘archipterygium’ by a process of freeing all the basals save the
most anterior one from contact with the margo radialis of the endogirdle
(Fig. 9B-D). This process was seemingly accompanied by admesial lepidotrichial
growth. At the same time, the primitively long endogirdle shortened
considerably and its contact with the inner side of the cleithrum was reinforced in
the double interests of serving increasing fin mobility and providing a greater
stability for the growing importance of the fin’s weight-bearing activities
(Andrews, 1973). These changes would have enhanced the flexibility of the
pectoral fin for the purposes of slow locomotion in keeping with the mode of life
(Thomson, 1969; Andrews 8c Westoll, 1970a, b).
The close similarity in lepidotrichial structure and arrangement in the fins of
all osteichthyans (Jarvik, 1948; Jessen, 1968; Denison, 1968a, b) together with
what has been said above on endoskeletal trends leads one to a picture of the
ancestral osteichthyan pectoral fin (cf.Jarvik, 1965). A scale-covered basal
muscular lobe subtended a lepidotrichial web. All the lepidotrichial rows were
jointed and branched. A fin-web of unjointed or unbranched lepidotrichia seems
only to be developed in fish which possess some other obviously advanced
characters (e.g. Turrasius; the haplolepids; the holurids; Belichthys, Hutchinson,
1975). Similarly, fringing fulcra are an advanced character (Gardiner, 1970).
From the usual comparability in structure between the pectoral and pelvic fins of
fishes, one may suppose that the paired fins in ancestral osteichthyans shared the
same general plan but this cannot be extended to the unpaired fins.
The ancestral bony fishes must have possessed heterocercal tails because this is
the only type found in the early members of the group. The evolutionary and
apparent ontogenetic history of the tail in the sarcopterygians (Thomson 8c
Hahn, 1968; Schultze, 1972, 1973) suggests that the development of the
epichordal lobe was a relatively late event. Primitively, the epichordal fin-rays
may have taken the form of ordinary scales covering the dorsal region of the
body-lobe of the tail, and these scales were transformed into dorsal fulcra and
NOSXV3d ‘MI ‘a
PRIMITIVE BONY FISHES
51
epichordal fin-rays in the actinopterygian and sarcopterygian lines respectively
(Jarvik, 1959; Gardiner, 1970). In both major lines the trend in caudal fin
evolution was the development of symmetry but there were at least four separate
mechanisms adopted by the different groups (actinopterygians: diphycercal and
homocercal ; dipnoans : continuous diphycercal; coelacanths : lobed diphycercal;
‘rhipidistians’: lobed diphycercal). Because of the presence of the axial lobe in
the Osteostraci, Acanthodii, Elasmobranchii and Palaeonisciformes (all with a
heterocercal tail), the development of the axial lobe (= subterminal lobe,
Thomson, 1976a) is probably functionally related to the heterocercal condition
and it was doubtless present in the ancestral bony fish.
The pattern of dermal cranial bones in the earliest osteichthyans is a matter of
controversy. In its essence, the argument turns on the question of the original
size of the elements concerned, were they micromeric, mesomeric, macromeric
or a mixture? The present consensus favours a mesomeric pattern developed in
association with the lateral-line canals and with anamestic micromeric units
inserted between them (Save-Soderbergh, 1934; Stensio, 1947; White, 1965;
Westoll, 1943, 1949; Schaeffer, 1968; Romer, 1970). A number of authors,
however, have been impressed by resemblances in the dermal head bone patterns
of the actinopterygians and crossopterygians and have supposed that the bones
in a number of areas (skull roof, operculum) were of fairly large size (Watson,
1925; Goodrich, 1930; Nelson, 1970a; Thomson & Campbell, 1971). The
dipnoan cranial ‘mosaic’, by this view, represents a development from originally
larger elements. This is the position supported in the present work (see also
Miles, 1975)and it is proposed to justifj it with functional considerations.
It has been suggested earlier (Pearson 8c Westoll, 1979) that the dermal
shoulder girdle was functionally related to the dermal skull rather than to the
pectoral fin in primitive bony fishes. Evidence for this contention includes the
nature of the dermal bones, which form an articulated continuous chain linking
the neurocranium (via the skull roof) to the massive cleithrum, where powerful
retractor muscles of myotome origin insert. Furthermore, in modern bony fish,
the greater part of the pectoral fin musculature originates on the endogirdle,
rather than on the dermal component (Romer, 1924;Jessen, 197213, 1973b).The
only bone of the dermal girdle which generally seems to be of importance in the
support of the pectoral fin is the cleithrum, yet it is likely that the major factors in
the determination of this bone’s form are the insertion of the retractor muscles
and the presence anteriorly of the branchial cavity, of which it forms the
posterior and medial walls. This is underscored by the presence in placoderms of
the very cleithrum-like anterolateral plate (Miles, 1967)which also apparently lay
behind a branchial cavity and constituted its posterior and medial walls.
If the single fundamental plan of the dermal pectoral girdle of osteichthyans
was established as part of the mechanics of skull action, then it seems reasonable
to suppose that the dermal skull pattern was established at about the same time.
I t is suggested here that the osteichthyan dermal cranium is fundamentally
macromeric in plan; it seems likely that the box-girder nature of the upper jaw
assembly in early actinopterygians and crossopterygians depends for its strength
and mode of action on large bony plates, as does the operculum. It therefore
seems unlikely that the intricate interplay of forces and function which
characterizes the osteichthyan jaw and gill skeleton continuum was independently acquired in separate lines each starting with a micromeric dermal
cranium. The dermal pectoral girdle has a single plan in the Osteichthyes (Jarvik,
i8
D. M . PEARSON
1944a) because its major function in the ancestral population was to retract the
skull to produce a wide mandibular gape. The design of the girdle, in the form of
generally large plates, reflected the acquisition of a head skeleton of similarly
large plates. The whole functional rationale for cranial retraction is a head
skeleton of predominantly large plates. In the nasal region, however, the mosaic
or series of small bones in the primitive members of all the lineages strongly
suggests that this was the original dermal cover in this particular area.
The long jaws of the osteolepid and rhizodontid crossopterygians and of early
dipnoans, as well as in the cheirolepids, probably mean that this is a primitive
feature of the Osteichthyes (Miles, 1977 :3 13).The underlying significance of this
character state is possibly the need for a substantial ventral surface area anterior
to the centre of gravity in order to gain lift by hydroplaning.
In their possession of a separate splenial (infradentary)series and the position of
the branchiostegal (submandibular) series lateral to the lateral gulars,
sarcopterygians (Fig. 7E, F) differ strongly from the actinopterygians. Jarvik’s
( 1963) suggestion that the submandibular series in the sarcopterygian lower jaw
represents a mandibular opercular flap is unconvincing on functional grounds. I t
seems more likely that these series are responses to sarcopterygian ecology and
orobranchial mechanics. With a kinetic cranium and a very flexible base to the oral
cavity, respiratory water flow could be maintained in a habitually stationay fish.
This would have been of especial importance in an environment which
experienced low oxygen tensions. The whole skeleton of the mouth cavity in
‘rhipidistians’seems designed around a central theme of great expansion capacity.
In early osteichthyans the gular region in all groups consists of large lateral and
small median elements. In palaeonisciformsand osteolepids there are two laterals
and a single median gular (Jarvik, 1944b, 1948; Fig. 7A, E). In dipnoans and
holoptychiids, additional flexibility may occur with both anterior and posterior
median gulars. The holoptychiids tend to retain the single large lateral on each
side (Fig. 7F), whereas the usual dipnoan condition (Urunolophus,Denison, 1968a;
Dzpnorhynchus,Westoll, 1949:fig. 5 ) is that these are each represented by two plates,
longitudinally arranged. It seems possible that in these two groups these are
devices to offset the consequences to the buccal-opercular pump of a shortened or
immobile palatoquadrate. This is almost certainly the case with, for example, the
conspicuously large operculum of the lungfishes.
I t is argued in the present work that of the major groups of the Osteichthyes, it
was the actinopterygians which retained the highest number of primitive features
in the skull (Gardiner, 1973).Not only do they lack the neurocranial and other
specializations consequent to the exploitation of either autostyly or the cranial
kinesis (the presence of a subcephalic muscle in Polypterus, Nelson, 1970b, being
probably a secondary condition, Schaeffer, 1973) but their dentition is similarly
unspecialized, being devoid of the palatal tusks or compound toothplates of
sarcopterygians. In the apparent functional emphasis on the palatoquadrate (as
opposed to the marginal dentigerous bones) in the feeding mechanism, the
sarcopterygians appear to share another (possibly specialized, Miles, 197 7 : 187 )
feature. This relative unimportance of the marginal tooth-bones seems to have led
to their reduction in size among the rhipidistians and to loss of certain of them in
Dipnoi and coelacanths (Denison, 1968b; Moy-Thomas & Miles, 197 1 ; Miles,
1977 : 187-8). The actinopterygianstherefore seem to retain the most unspecialized
feeding mechanism among the Osteichthyes. On the grounds of linked function,
this statement probably can be extended to cover the branchial apparatus,
PRIMITIVE BONY FISHES
59
operculogular system, dermal cheek and pectoral girdle also. We may therefore
suppose that the head of ancestral bony fishes was built along generally
actinopterygianlines.
Arising out of the phenomenon, common in early gnathostomes, of
enlargement of the forebrain region (Schaeffer, 1975) with a correlated extension
of both neurocranium and the dermal roofing bones (frontals) in this area, the
relative length of parietals to frontal has been used on occasion as a rough
estimate of primitiveness within the Osteichthyes (e.g. Rayner, 1951). The relative
shortening of the parietals (Figs lA, B, 3, 10) is taken very far in some
actinopterygianswhere the posterior border of the frontals may actually come into
contact with the extrascapulars (Fig.3E, F) but it also occurs to a lesser extent in the
rhipidistians (Fig. 1OA-C; Jarvik, 1967; Panderichthys, Worobjeva, 1973) and the
Dipnoi where it is observable as a prepineal extension and a postpineal
sc
Figure 10. Skull roofs of sarcopterygians, showing progressive shortening of the posterior region of
the skull and extension of the anterior region. In D and F, the position of the pineal organ is beneath
bone D. Not to scale. A, Osteolepis macrolepidotus (afterJarvik); B, Eusthenopteronfoordi (afterJarvik); C ,
Eu&nodon sp. (after Jarvik); Urunolophus wyomingensis (after Denison); E, Dipnorhynchus tursmilchi
(afterDenison);F, Dipterw ualenciennesi (afterDenison fromJarvik).
60
D. M . PEARSON
abbreviation in Uranolophus - Dipnorhynchus - Dipterms (Denison, 1968b;
Fig. 1OD-F). Among actinopterygians, only Cheirolepis (Fig. lA, B)and Moythomsia
nitida (Fig. 3A) have frontals and parietals of equal length and this is obviously
either the primitive state or an indication of an earlier condition where the frontals
were shorter than the parietals.
The evidence afforded by early osteichthyans and their general evolutionary
trends can be accounted for most economically in the following outline of
osteichthyan adaptive radiation : the actinopterygians retained many of the
features of the primitive osteichthyans : the small scales, general cranial
niorphology and the keel-like, rather inflexible fins. They successfully exploited
the open waters of the Lower Devonian and refined the locomotory mode of their
micromeric ancestors into a ‘selachian’ type of continuous economical swimming.
This involved a mobile trunk and to this end the anterior dorsal fin, with its
property of resistance to the trunk movements in the yawing plane, was eliminated.
The sarcopterygians exploited shallow, turbid water bodies and lost the habit of
swimming for any extended periods of time. The two dorsal fins of the ancestor
were retained in the interests of directional stability for the anterior part of the
trunk and so helped to make sudden bursts of powerful, accurate locomotion
possible. The scales enlarged and the strength of the scale-rows in compression
was increased : this improved the role of the scale-row in bracing the sides of the
trunk and so preventing twisting of the body under power and maintaining
locomotor accuracy.
AJffinities of the bony jishes
An argument has been developed above for an ancestral osteichthyan
morphotype. What of its own ancestry?
Of known agnathans, while there are some suggestions of a pregnathostome
organization in the Heterostraci (Halstead, 1973a, b), all seem barred from the
ancestry of any gnathostome group on the grounds of general cranial and
branchial anatomy (Stensio, 1964). The placoderms are unsuitable for the same
reasons (Stensio, 1959, 1963; Gross, 1962; Schaeffer, 1975).The only group able
to be considered in this role are the earliest known gnathostomes, the Acanthodii.
The current consensus concerning the phylogeny of the group, as noted above, is
that they represent a group collateral to the Osteichthyes, but a minority opinion
(Heyler, 1958, 1962; Schaeffer, 1968) proposes a directly ancestral relationship.
The most significant of the resemblances between the acanthodians and the
bony fishes (see also Miles, 1965) are as follows:
( 1) The neurocranium is built along the same lines in both groups, with anterior
and posterior dorsal fontanelles, lateral occipital and ventral oticosphenoid
fissures (however, acanthodian data are necessarily derived from the
degenerate Permian survivor, Acanthodes).
(2) There are strong resemblances in the structure and support of the palate in the
two groups (Schaeffer, 1975), e.g. the close association of the hyomandibula
with the posterior edge of the palatoquadrate. The primitive acanthodian
suspension may have involved just the hyomandibular and palatobasal
articulations, both of which are present in the Osteichthyes (apart from the
lungfish where there is secondary autostyly).
( 3 ) The dermal skeleton has a similar histology in acanthodians and
osteichthyans. In both groups the basal layer is of bone, either acellular or
PRIMITIVE BONY FISHES
61
cellular. Above this occurs the dentine (spongiosa)layer which is penetrated by
blood vessels. In acanthodians the external surface of the scale is formed by
this dentine, while in osteichthyans this takes the form of a third layer,
enameloid. What direct evidence there is supports a hypothesis of the ancestor
of the osteichthyans possessing a bilayered bony scale devoid of superficial
enameloid, such as occurs in the acanthodians.
(4) In both groups the cranial exoskeleton primitively included flexiblyarticulating medium-sized dermal bones.
To what extent parallel evolution is responsible for these apparently significant
resemblances cannot presently be assessed. There has, however, been considerable
parallel evolution between actinopterygians and post-Silurian acanthodians. Thus
both groups show a loss of the anterior dorsal fin, an increase in fin mobility and a
general reduction in dermal ossification. Furthermore, acanthodians appear to
develop (Miles, 1965, 1966) an operculate branchial chamber in the course of the
Devonian and a basisphenoid region marked by a rather posteriorly-sited ventral
otic fissure.
There are two major objections to the acanthodians as osteichthyan ancestors :
their spinous precaudal fins and their lack of dentigerous dermal bones around
the jaw and gill apparatus. It proves nothing to speculate about whether these
character states . are capable of transformation to their osteichthyan
manifestations along the gradient of continuously increasing benefit that
evolutionary theory demands. One may note, however, that in the single plan
apparently displayed by osteichthyans in the dermal skeleton of the head, pectoral
girdle and the fins, there are suggestions that the inception of the bony fishes was
marked by radical improvements in cranial dynamics (both respiratory and
feeding) and locomotor control. Therefore it seems that any ancestor of the
0steichthyes may be expected to differ markedly from their descepdants in these
regions. Furthermore, the wide range of dentition morphology displayed by the
Devonian acanthodians (Watson, 1937; Miles, 1966; Orvig, 1967, 1973; MoyThomas & Miles, 197 1) indicates an earlier period in the evolution of the group
when considerable dental innovation occurred, with the subsequent exploitation
of the peculiar advantages of the different patterns by different lineages.
Other acanthodian features distinguishing them from bony fishes, such as the
path of the lateral-line canal of the body between rather than through the scales,
and differences in the branchial skeleton (Nelson, 1968; Gardiner, 1973) are not
considered weighty. In the matter of the gill-skeleton, for example, there seems to
have been a considerable improvement in both the oral and branchial moieties
of the orobranchial pump in ancestral osteichthyans, so contemporary alterations
in the gross branchial structure are to be expected.
Any discussion of acanthodian-osteichthyan relationships is further hampered
by the rarity and fragmentary nature of the early (Silurian) acanthodians. At
present there does not seem to be any way to discriminate between primitive
acanthodians and their own (unknown) progenitors as osteichthyan ancestors.
CONCLUSIONS
( 1 ) Cheirolepis canadensis (U. Devonian) may be regarded as a derivative of the
slightly earlier (M. Devonian) C. trailli. In some characters, such as the dermal
cheek ornament, C. canadensis is more advanced than C. trailli, paralleling
mainstream palaeonisciform trends. Some of the distinguishing characters of
C. canadensis stem from its larger size.
62
D M . PEARSON
(2) In such characters as scale size and arrangement, parasphenoid shape,
suspensorium angle, the architecture of the gular region, palatoquadrate
structure, pectoral endoskeleton, circumorbital and nasal exoskeleton,
Cheirolepis retains much of the morphology of ancestral actinopterygians.
(3) In its generally archaic suite of characters, Cheirolepis appears to be at a
distinctly lower level of locomotor evolution than the typically ‘large-scaled’
palaeonisciforms. In its fossil occurrence, the genus is probably a late survivor:
it is supposed that animals of its organization were more typically Lower
Devonian, or perhaps even earlier.
(4)There are no features in the structure of Cheirolepis debarring it from a position
of ancestry of the stegotrachelid palaeonisciforms. There are no features in the
structure of the stegotrachelids debarring them from a position of ancestry to
later palaeonisciforms.
(5) The Osteichthyes are considered to have initially radiated into actinopterygian
and sarcopterygian lines. The unique structure of the osteichthyan dermal
cranium makes it clear that the development of its fundamental plan was an
early and important event in the history of the group. At one time there was a
population of ancestral bony fishes with a head of this plan. The mechanical
functioning of the dermal skull required medium- and large-sized bones.
Intimately related to the operation of the head was that of the dermal pectoral
girdle, whose single plan in the Osteichthyes reflects an original single function
allied to the single cranial dermal bone pattern of medium and large bones.
( 6 ) Of the major groups of the bony fish, the actinopterygians resemble the
ancestral morphotype the most, having deviated least from the primitive freeswimming mode of life. The sarcopterygians took up a rather stationary
existence in shallow muddy water and the feeding mechanism, the fin and
girdle structure and the gross and fine scale structure all became modified in
the interests of success in this environment.
( 7 ) The acanthodian fishes show most of the features one might expect to occur in
an ancestor of the Osteichthyes. The squamation of Cheirolepis is an inheritance
from either primitive acanthodians or acanthodian progenitors.
ACKNOWLEDGEMENTS
I am indebted to Professor T. S . Westoll for introducing me to the fascinating
topic of the primitive bony fishes and, by numerous conversations, providing
much of the background for this paper. I thank also all the friends and colleagues
with whom I have discussed aspects of fish evolution, especially Drs R. L. Paton, B.
G. Gardiner (who read an early draft of this paper), C. Patterson and L. B.
Halstead. My grateful thanks go also to the Natural Environment Research
Council, whose award of a studentship made the original study possible; and
finally to DrJohn Banks, then of the University of Liverpool, who showed me that
rationale for structure is function.
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ABBREVIATIONS USED IN FIGURES
aPa
aPP
A.Pr
Cen.c
c1
Cth
D
D.Hy
DSP
Exsc
F.pin
Fr
Gu.1
Gum
It
Ju
L.Pr
Md
M.Pr
Mx
anterior ascending process
posterior ascending process
anterior posaostral
central laterosensory canal
clavicle
cleithrum
dermal bone directly over pineal organ
dermohyal
dermosphenotic
extrascapular
pineal foramen
frontal
lateral gular
median gular
intertemporal
jugal
lateral postrostral
mandible
median postrostral
maxilla
Na
0
OP
Op.Acc
oscl
Peg
Pa
Po
Podsp
POP
P.Pr
Pro
P.tem
RBr
S
SOP
SP
SPO
St
nasal
position of orbit
opercular
accessory opercular
orbital sclerites
articulatory peg of scale
parietal
postorbital
postorbito-dermosphenotic
preopercular
posterior postrostral
preorbital
post-temporal
branchiostegal ray
articulatory socket of scale
subopercular
spiracular opening
supraorbital
supratemporal