~oologicalJourna1ofthe /.inneon Sociefv (19821, 75: 167 -188. With 1 figure
What are the ‘Calcichordata’?
and the larger question of
the origin of Chordates
MALCOLM JOLLIE
Riological Sciences, ,i\brthein ILlinoiJ Universip,
D e K d b , Illinois 60115, LI.S.,-l.
Argiiment aroiind the qliestion o r t h r validity of the ‘(hlcichnrdata’ emphasizes the need fi>ra more
functional and utilitarian view of the origin of the chordates. The calcichordate question is reviewed
and ‘tested’ in terms of our tisu;il ideas of biological reality. The concept is rejected and the Stylophora
are viewed as aberrant and still largely unknown echinoderms. Rejection of the calcichordate concept
turns us once more to the question of the origin nf the chordates. .4 number of competing hypotheses
are cornpired: the tiinic;ite, dipleuruloid and ;irchicoelomate models. The conclusion is that the
dipleuruloid. ;I simple metazoan, offers the least explanatory difficulties. Also it is concluded that
discussion of such a subject as this refines and improves our thinking concerning it.
KEY WORDS :-C;ilcichiirdates
Stylophora
;irchicoelornate phylogeny origins.
~
echinodrmls
chordates
tunicates dipleuruloid
~~
CONTENTS
Introduction . . . . . . . .
Mrthod . . . . . . . . .
Iliscussion . . . . . . . . .
Jefferirs’ hypothesis . . . . .
The echinoderm affinity of the Stylophora
Tunicate hypothesis . . . . .
llipleuruloid hypothesis . . . .
Archicoelornatr throry
. . . .
Summ;ition
. . . . . . . .
,2rkriowledgeriierits.
. . . . . .
References.
. . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . .
. . .
. . .
. . .
. . .
167
168
169
169
173
175
179
182
185
186
186
INTRODUCTION
Jefferies (1967, 1968) identified the Stylophora as a group of echinoderm-like
organisms, the Calcichordata, which he believed were ancestral to the chordates.
Since then he has published a series ofpapers attempting to clarify and establish his
claims. I (Jollie, 1973) have commented on Jefferies’ ideas, as have Eaton
(1970a,b), Ubaghs (1975) and Philip (1979).Not all comment has been negative
(Eaton, 1970a; Paul, 1977). Generally, this new grouping has gone with little
+
0024- 4082/82/060167 22303.00/0
167
01982 The Linnean Society of London
168
M. JOLLIE
comment, but such an important concept should generate more interest and
concern than it has. Why then have Jefferies’ views not been discussed more
widely ?
A study of phylogenetic arguments is a lengthy and complex operation (see
Philip, 1979). This is not a narrow specialty, like those to which most biologists
address themselves-nor
can its basic tenets be reduced to some simplistic
formulation. Jefferies has argued his thesis, modified from Gisltn (1930), by way of
several hundred pages and in anatomical detail far beyond the capabilities of most
zoologists or comparative anatomists. Contributing to this problem is the fdct that
this is an area of zoological research which is largely neglected. Neglect has led to
failure to publish review articles on the origin of groups, including the chordates,
and, especially, to update general accounts. For invertebrate zoologists, sources
continue to be the Handbuch der <oologie, Grassk’s TraitC de <oologie or
Libbie Hyman’s volumes ( 194c1967). The Treatise on Invertebrate Paleontology (ed.
R. C. Moore-see Ubaghs, 1968) gives the paleontological view. As a result, an
evaluation of such a question as the origin of a phylum is difficult.
I n part, this difficulty stems also from current philosophy. I n such theoretical
matters, most biologists take either a wait-and-see stance (actually one of let
somebody else do i t ) , or they are loud in condemnation of such ‘unscientific
speculations’. It is my personal view that the realm of science continues to expand
into ‘metaphysical’ areas as our ability (or willingness) to deal more objectively
with facts and ideas improves. Another aspect of a problem such as this is
understanding and interpreting information. In this respect, I present my ideas as
to what various authors have said and they may not necessarily agree with me. The
time for phylogenetic speculation is now if we are to continue our advances in the
understanding of the course and method of evolution.
The question of the relationship of the ‘calcichordates’ is a part of the overall
problem of the origin of the chordates. Any consensus on the nature of the
Stylophora must be compatible with a general theory of the origin of chordates. It
is precisely because this last is lacking inJefferies’ approach that I reject the idea of
a chordate affinity of the Stylophora and support their echinoderm nature.
Although I agree they are very strange echinoderms!
METHOD
The best approach to an evaluation ofJefferies’ view, or any speculative view on
origins, is to contrast it with other alternative and competitive explanations. In
such an approach, ‘testing’ is done by observing the relative explanatory value of
each scheme and the relative amount of friction with basic biological concepts (of
embryology, morphogenesis, adaptation, genetics, etc.), The test is the ‘fit’ into
the pattern of ‘known’ evolutionary information. For example, one should question
the origin of one group from another of equal but different complexity. The
adaptive change necessary for transition demands extensive restructuring that
is incomprehensible in terms of evolutionary theory. Such an origin also has little
informational value in that attention is merely shifted to the origin of the
complexity of the ancestral group, In this review, a limited array of ‘theories’ will be
contrasted-not all theories are considered worthy. An outline will be presented of
Jefferies’ hypothesis and the alternative view of the echinoderm affinity of
stylophorans. Neither of these treats the origin of chordate structure which will
WH.\T .\RE ‘C.41~CICHORDAT.4’2
169
then be probed by way of the currently popular tunicate theory, my own
dipleuruloid scheme, and the ‘archicoelomate’ concept of Gutmann. One might
wonder why a criticism ofJefferies’ views would not suffice, but evaluation rests on
other assumptions (not considered by Jefferies) which come under scrutiny in these
otherwise disparate discussions.
Thus, this paper will be an attempt to portray the main components of each of
the se\.eral schemes, as I am able to interpret and assess them. The argumentation
is often so complex that the thread may be lost; or the interpretation can be
distorted or e\.en in error. Fine shades of difference, not necessarily to be gained
from the language used, have often been the cause of great disputes. It can be
assumed at the start that none of these schemes is totally wrong in its thinking and
use of ficts and probably none is totally right. An eclectic spirit is needed.
DISCUSSIOS
Jgferies’ hypothesis
(drawn mainly from his paper of 1975 and Jefferies & Lewis, 1978)
Calcichordates, represented by cornute and mitrate fossils, usually identified as
carpoids belonging to the phylum Echinodermata, are in fact more closely related
to the chordates and are ancestral to that group.
Derdopment of /y/iothesi\
( 1 j Segmentationist (derived from a segmented swimming ancestor) and antisegmentationkt (deri\red from an unsegmented tunicate tadpole) standpoints are
compatible, “. . . the uniformly segmented protovertebrate of the segmentationist
school . . . descended from the antisegmentationist protovertebrate” Uefferies &
Lewis, 1978:308).
(21 The mitrates are the stem group from which have evolved, as separate lineages
in the Upper Cambrian, the tunicates, amphioxus, and the agnath vertebrates.
The mitrates continue into the Devonian as the Anomalocystitida.
( 3 1 The mitrate is basically a tunicate-like filter feeder with a capacious pharynx,
bilateral atria and 21 loop gut (opening into the left atrium) ; the tail has a dorsal
nerve, notochord, and segmental muscles.
(4)The conversion of a mitrate into a vertebrate involves a number of changes:
( a )De\relopment ofthe head is by expansion posteriorly below the anterior part ofthe
tail. The mitrate head consists of premandibular and mandibular segments (the
premandibular behind the mandibular!) in which are found the pharynx, viscera
and atria. Expansion of the head posteriorly has created hyomandibular,
glossopharyngeal and \raga1 somites by extension of the pharynx below the stem ;
the viscera ha1.e moved even more posteriorly to give rise to a ‘trunk’. T h e atria
were con\.erted to the branchial chambers of the ‘operculate’ vertebrate. T h e otic
\vesicle, originally in the atrium, now moves through (‘crushes’) the
hyomandibular somite, moving back and dorsally. The eyes ( cispharyngeal pairor the tr;inspharyngeal pair) lie in association with the brain, just anterior to the
notochord but behind the pharynx. The nasal organ is located at the margin of the
mouth, which opens terminally.
( b ) An animal that crept backward by means of a stubby, hooked tail now began
to swim forward by means of the same, but now finned, tail.
170
M. JOLLIE
(c) The transition is assumed to have involved the loss of the ‘calcite’ skeleton,
followed by a naked phase, followed by development of a bony skeleton
(resembling the original calcite plate cover!).
(5) Conversion of particular genera of mitrates into tunicates and amphioxus
proceeded directly, with many details of the descendant group already present in
the ancestor.
Style of argumentation
There is little question that this is a largely traditional type of argument
involving also the method of Stensio in which detailed reconstruction of a fossil is
carried out, using an assumed living relative to supply the detail; the resultant
resemblance is then used as proof of the relationship. Again, comparisons are made
which can only be described as questionable. Jefferies has not really addressed the
problem of the origin of the chordates, only the conversion ofmitrates to the several
subphyla of chordates.
Samples of the argumentation are revealing as to his thinking. As a first
example, he says Uefferies & Lewis, 1978 :308) : “The neural gland of mitrates was
probably situated beneath the prosencephalar part of the brain and its duct would
have run forward to open into the left pharynx just anterior to the dorsal meeting
place of the left and right peripharyngeal bands. It was therefore situated much as
in a tunicate tadpole.” One would prefer that “probably” be left out of this
statement and that the assumed prosencephalar part of the (vertebrate) brain not be
compared with the vesicle of a tunicate. He suggests Uefferies, 1975:268) that
“The gonopore and anus migrated to left of the tail in Cothurnocystis, so as to be
behind the gill slits, where faeces and gametes could be washed by the branchial
current.’’ This suggests (Jefferies, 1968:246) that although “. . . a functional
explanation has been sought for as many features as possible,” the account does not
explain where the anus migrated from or how it got there in the first place. The
‘looped’ gut of the tunicate does not compare with the straight gut of the embryo
vertebrate, with its anus near the neurenteric canal (before postanal extension of
the tail).
Describing these fossil forms as chordates, he noted Uefferies, 1968 :246) that
“The results flatly contradict the idea of a completely segmented vertebrate
ancestor with mandibular and premandibular gill slits which is so firmly
embedded in classical vertebrate anatomy .. . but for which the evidence is, in fact,
very weak .. .” But, he is not clear how or why Uefferies, 1978) the multislitted,
asymmetric carpoid is converted to the ‘classic’ vertebrate with simple symmetrical
slits. Again, he commented Uefferies, 1975:283) “The origin of the right pharynx
and right gill slits is an all-or-nothing process which could only have happened
between one generation and the next. The first mitrate, defined as the first
chordate with right gill slits and right pharynx, would have been a ‘hopeful
monster’ and the child of cornute parents.” It would indeed require a hopeful
monster to convert an organism with the ‘brain’ posterior to the gut (Jefferies,
1975 :289) to one with the chordate relationships.
Jefferies Uefferies & Lewis, 1978:214) defends his view with a number ofgeneral
statements :
( I ) Agreement with the classical theory of an echinoderm relationship. His
contribution involves a clarification of the nature of that relationship.
WHAT ARE ‘CALCICHORDATA’?
171
(2) The remarkable similarity in structure with tunicates. He stated Uefferies
1975:264) “. . . the comparison of the pharyngeal structures of mitrates with those
of tunicates is now so strong and detailed that there can be little doubt of the
correctness of the basic chordate interpretation of these animals.”
( 3 ) The asymmetries, such as only left slits being present in cornutes as in larval
amphioxus, or the anus opening into the left atrium in mitrates just as in ascidian
tunicates, are like those of chordates.
(4) The evidence of dorsal nerve cord, notochord, muscle blocks, brain and cranial
nerves ‘clearly’ makes these animals chordates and close to vertebrates.
Criticism of the hpothesis.
It seems appropriate to include the above statements as generalizations leading
to the hypothesis.
Echinoderm telationship. I would provisionally accept some of Jefferies’ views as to
the internal anatomy of calcichordates, but would balk at much of the detail such
as ‘eyes’ or ‘neural gland’. If the calcichordates are viewed as animals with a
terminal mouth (usually large) and large pharynx (or is it just a capacious stomach
or even a vestibule?), then they are distinct from echinoderms (as he states). The
occurrence of pharyngeal slits through the body wall in Cothurnocystis may be a
correct observation, but this would not necessarily closely link the group with
hemichordates, tunicates, amphioxus, or vertebrates. The lack of a water vascular
system strikes me as very important and suggests that the group separated from the
main echinoderm line before the appearance of that system. I suggested Uollie,
1973:86, continued as lines 4-14, right column p. 85) that the primitive
echinoderm lacked a water vascular system. Comparison with the solute (Kolata,
1973; Kolata, Strimple & Levorson, 1977), is interesting as solutes are apparently
typical echinoderms with a water vascular system and an arm. (Paul, 1977, notes
the occurrence of the water vascular system in Lower Cambrian echinoderms.)
The body plan of the calcichordate, ‘theca’ and ‘stem’ is like that of an
echinoderm, as are the calcite plates (Caster & Eaton, 1956).Jefferies’ early study
led to the conclusion that the tail of the calcichordate and the stem of the crinoid
wcre homologous (later disavowed but without real change in argumentation).
True the ‘tail’ of the calcichordate is highly modified as it was used, presumably, in
locomotion. The calcichordates seem, thus, closer to echinoderms than to
chordates with which they share no basic features in terms of the known hard
structures.
Jefferies’ assumption or reaffirmation of a classical theory of echinoderm
relationship is misleading in that the classical view is not a comparison of a carpoid
with an ostracoderm but rather is based on similarity of larval structure which
leads through the hemichordates to the chordates.
Tunicate similario. The alleged tunicate similarity of mitrates is largely a result
of Jefferies’ reconstruction. I have grave doubts that the few ridges, grooves and
pits can be interpreted in such detail. Jefferies’ basic assumption is that the mitrate
is like the tunicate tadpole larva, the tail ofone comparable to the tail of the other.
The pharynx and gut of the tunicate are those of a sessile, filter-feeding organism,
not of an active ( ? ) organism such as the calcichordate. There is no evidence that
tunicates stemmed from an organism that lay on the sea bottom as did the
Calcichordata. Tunicates lack evidence of a calcite skeleton, whereas loss of such a
I72
M. JOLLIE
skeleton and substitution of a tunic does not make much phylogenetic sense as the
body wall of the tunicate is elastic and can be contracted by muscle. Other
criticisms of the tunicate approach to chordates are given below.
Asymmetries. Jefferies’ ideas of asymmetries stem from comparisons of
hypothetical soft parts with structures seen in tunicates and amphioxus; these are
ideas that cannot be dealt with effectively. In thinking about evolution, the general
consensus is that symmetry precedes asymmetry, and there should be little question
of the bilateral nature of the chordate ancestor and the probable distortion of this
as a result of attachment for filter feeding or burial in sand for filter feeding; or, in
the case of the larva of amphioxus, modification for feeding. Similarly the
asymmetries of the calcichordates are probably a consequence of the modification
of a sessile, stalked, echinoderm-like ancestral form to one lying on the bottom,
with top and bottom sides. The asymmetries of the calcichordates are probably,
like those of tunicates and amphioxus, equally secondary and independent. Until
we know something of the feeding mechanism of this group nothing more can be
said.
Presence of notochord and nerve tube. Actually no effort is made to account for these
structures. Jefferies’ original comparison of the calcichordate ‘tail’ with the crinoid
stem may be valid, but he abandoned that comparison (because of Eaton, 1970b)
while retaining the comparison with the chordate tail ; this indicates the confused
nature of some of the argumentation. He stated Uefferies, 1975 :264) “Comparing
a calcichordate tail with a crinoid stem, though probably dependent on parallelism
[convergence] rather than homology, was less misleading than comparing it with a
crinoid pinnule. For tail and stem both arise from the same posterior or aboral pole
of the animal”. (It would seem that a comparison of tail and crinoid stem still has
some value!) “The conclusion, therefore, that stems and tails are parallels rather
than homologues does not greatly alter the arguments for connecting
calcichordates with other chordates, which are now confirmed bv detailed
resemblances of their pharyngeal structures with those of tunicates” (Jefferies
1975: 255).
His comparison of tail and stem led to the idea that a notochord was present in
both. He noted Uefferies 1975 :255) : “There is functional-morphological evidence
that the tail of calcichordates contained a notochord, and direct evidence of a
dorsal nerve cord overlying this notochord.” He nowhere accounts for the
notochord as a functional structure. (What is its value in a ‘tail’ ofarticulated hard
parts?) All this from a study of impressions, gooves and ridges which I find hard to
take seriously. T o make matters worse he commented Uefferies, 1975:263) :
“There is circumstantial evidence that a main blood vessel passed down the middle
of the notochord”. I cannot help but reject these comparisons with the chordate
tail; therefore, notochord, nerve tube, and segmental muscle, at least homologous
ones, are lacking and without these homologies the whole argument collapses.
Even worse, he assumes that the mitrate ‘tail’ is only partly homologous with that
of the cornute!
Conversion dfjculties. Jefferies’ steps in the conversion of a mitrate to a vertebrate
are far too complex to be acceptable. One would hope for more parsimonious
arguments, firmly associated with functional, adaptive considerations (things that
could be selected). Surely the vertebrate head is best characterized by its symmetry
and the strong development of the several visceral arches, each served by
characteristic nerves and blood vessels. None of this is seen in the presumed
WHAT ARE ‘CAIXICHORDATA’?
173
calcichordate ancestor (nor, for that matter, is the presumed resemblance in
external form of this ancestor and the armoured agnath vertebrate very real).
Jefferies assumes that the body of the calcichordate included two segments (for
which there is no real evidence) : the premandibular and mandibular. Bjerring
(1977) would be displeased with this view because he believes there is at least one
more segment anterior to the premandibular. I am unhappy with Jefferies’ view
because I believe that the mouth opens behind the premandibular segment, not
through it. The stem (tail) can be viewed as segmented but not in a way different
from that of a crinoid. There is thus no real reason to view the carpoids as
“segmented”.
Change in habit. It is not clear why a relatively inactive benthic group had
L‘
eyes”-not one but two pairs, and these on what I would identify as the ventral
side (also Philip, 1979:47 1 ). The complex nervous system described by Jefferies
and compared with that of the vertebrate agrees better, at least superficially, with
that of a crinoid. A postpharyngeal brain just does not convert easily into that of a
vertebrate. The suggestion that the tail of the mitrate became a swimming tail does
not seem probable. There is the matter of reversal of direction of movement, n
matter ofaltering the muscles used in hooking the tip of the tail down and forward,
and the problem of the origin of the caudal fin. Total rebuilding of the tail would
be required to produce enough force to move such an organism (even if naked!).
Jefferies argument is made even more difficult in that, in spite of the obvious
similarities of the “tail” and the homology of the cornute strut and the oblique
internal ridge of the mitrate, he turns the mitrates upside down in order to get an
advantage in his interpretation (see Ubaghs, 1975 :87). Philip (1979) rejected
J efferies’ view.
T h e echinoderm afinity of the Stylophora
(Ubaghs, 1967, 1968, 1975; Caster, 1968, 1971)
The stylophorans (‘calcichordates’), are in fact peculiar, early, nonpentamerous echinoderms with no evident closer relationship to the chordates than
that.
Derielopment of hvkothesis
(1)The skeletal parts preserved are calcite crystals similar to those of living
echinoderms.
(2) The Stylophora are pre-pentamerous, triradiate derivatives of an early
pelmatozoan. There is no evidence of a water vascular system.
( 3 ) The ‘stem’ is identified its a stele which may be subvective (locomotor) in
function or act as a feeding arm, an aulacophore, or both. It is not the homologue of
the pelmatozoan stem.
(4) A problem (Philip, 1979) is that the only consistently present opening through
the body wall has been identified as the mouth (Jefferies) or anus (Ubaghs,
Ciister). The suggestion is made that this opening served a vestibule into which
both mouth and anus opened.
St vle of‘ a rg urn entat ion
‘This is ii traditional argument based on broad similarities rather than fine detail
or functional arguments. Ubaghs (1975:86) stated “The skeleton of an
I74
M. JOLLIE
echinoderm is so peculiar that it is highly improbable that this type of skeleton
could have evolved in more than one phylum. . . . The Stylophora had an
echinoderm-like skeleton simply because they were echinoderms.” Further he
notes “An anal pyramid resembling that of many fossil and living echinoderms [is
present] . . . It is, however, so obviously the vent that such an experienced specialist
ofechinoderms as Bather (1913) took it as the starting point of his interpretation of
the stylophoran genus Cothurnocystis.” (It is this ‘anal pyramid’ that Jefferies
identified as the mouth.)
The stele or aulacophore is a basic component of this pre-pentamerous group.
Ubaghs and Caster assumed that the cornute and mitrate have the same
orientations (similar dorsal and ventral sides) and that their steles are homologous
and of similar structure. Jefferies saw these as stems broken off, although there are
fossil steles for both groups that taper to a point. According to Ubaghs (1975:86)
this stele resembles the food-collecting arms of extant ophiuroids, a point on which
most observers would disagree with him. However, he noted that the various
apophyses, grooves, and ridges on the inner side of the theca may be interpreted in
echinoderm terms (not done convincingly), whereas none unequivocally indicated
that they housed chordate structures such as a brain, notochord, or an axial nerve
cord. Ubaghs argued that the distal part of the stele has characteristically bilateral
rows of ‘cover plates’ which would allow it to be used in feeding. This would
necessitate that the food groove become a tube in the stylocone and in the
muscular proximal part. Jefferies (and Kolata and Jollie) have pointed out that the
‘cover plates’ in some steles are articulated in such a fashion that they could not
open out. The open position seen in many fossils is a secondary state due to some
disarticulation. The question of the stele, aulacophore or stem, remains, but
certainly this structure does not closely resemble the ‘stem’ of the solute, or Cincta.
Caster (1971 :920) has summed it up. “Neither Ubaghs or the reviewer takes
any stock in Jefferies (1968) theory that the stylophorans represent a
subphylum Calcichordata of the Chordata. To us, the ‘carpoids’ as a whole are in
every detail of gross morphology and skeletal histology echinodermal.
Consequently, for us, all the relevant homologies are with other representatives of
that phylum. Such similarities to chordates as ‘carpoids’ possess are in our view
wholly convergent and analogous.” Ubaghs (1975 :87) concluded “There is
certainly no sufficient reason for doubting the Stylophora were real echinoderms.”
Criticism of the hypothesis
Caster noted that “. . . ‘carpoids’ . . . are in every detail. . . echinodermal” but does
not confess to the fact that few details are known. The fact that only one body
opening is known for sure is not stressed. If this is the anus, then the mouth is
assumed to be internal at the base of the ‘stele’. This last can only be conjectural.
In this regard little attention is paid to the fact that in Lugynocystis there is, in the
‘posterior’ (stele end) extreme of the body a partial screen of ‘calcitized bars’ which
lies inside the dorsal transverse opening between the base of the stele and the body
cavity. What would be the function of such a screen near the mouth (or anus)?
The other openings described by Jefferies are not consistently observed throughout
the Stylophora and are, therefore, poor candidates for mouth or anus.
In contrast to the distinct anal pyramid of the cornute is the wide aperture of
some mitrates, margined dorsally with narrow plates. This large opening appears
WHAT .4RE ‘C:\I~CICHORD.\I’.~’?
I75
to ha\re been associatcd with some sort ofcavity and may haire ser\.ed both mouth
and anus.
The prolilem of the stele is not soh-ed and to argue one way or the other does not
bring i t closer to soliltion. ‘I’he lack of a water \.ascular system is suggesti\.e of an
early origin (pretriradiate?),an origin before the establishment of that system or at
least its conspicuous de\relopment in echinoderms. T h e fact remains that the
stylophoran is yet an enigma e\.en though one concludes that it is an echinoderm.
This comparison of ;i chordate or echinoderm association of the Stylophora
fkivours the later. A chordate association is radical and appears to be based in the
final analysis on the shape of these organisms and their skeletal features. Neither of
these, nor the many details hypothesized by -Jefferies can actually be used to
support a chordate relationship. If the chordates did not stem from the
stylophorans what sort of origin should be assumed? I will consider three theories :
the tunicate, dipleuruloid and archicoelomate.
Further consideration of the problem of the Calcichordata rests on an
understanding of other \.iews its to the origin of the chordate and something of the
nature of the primiti\.e chordate. U’as this ancestor in fact echinoderm-like?
T u nica t~ hypot h esis
(taken basically from Garstang, 1928)
A sessile, trinicate-like, non-chordate organism evol\red an actikve 1an.a with
notochord and dorsal nerve tube a s parts ofits swimming specialization. This larval
form, by neoteny, increased in size, de\reloped segmental muscle blocks and
gradually e\.ol\.ed into a vertebrate.
Der~~lopment
oJ hvfiothe.ri.r
( 1 j The ancestral ‘tunicate’ was a pterobranch-like, sessile organism. T h e feeding
mechanism in\wl\.ed passing water (by ciliary force) through the mouth and out
t h roil g h pha ry ngea 1 sl i t s .
(2 I The 1:m.a of this sessile organism was an i1ctii.e one swimming by means of its
ciliated belts. 12’ith increase in size, i t gradually elongated and began to swim by
muscular undulations. This modified larva had ;I ‘dorsal’ concentration of nerve
tissue (which in\.aginated a s a tube), bilateral muscle bands along the length of the
llody and a notochord (Garstang, 1894). ( A second scenario is that the early lar\.a
developed at a single step a swimming tail with unsegmented muscle strands, notochord and dorsal nerve tube-Berrill, 1955. Only later, in this second scenario,
(lid the musculature become segmented.) ’This larval stage became the
reproductive stage of the protovertebrate and the former sessile adult was
eliminated from the life cycle.
( 3 I The ascidian tiinicate 1ari.a retains much of the transitional structure of this
hypothetical ancestral organism; transitional between the sessile, tunicate-like
beginning and the vertebrate.
(41 ‘I’lle early vertebrates were filter feeders similar to the tunicate (or
amphioxus--and all ha\.e homologous pharynges i, but may ha\re lacked atria ; or
modified the atria to branchial chambers.
S t y l e qj arpmentation
A s with Jefferies, the argument utilizes anatomy, de\relopment, and the
‘comparative approach’. It a&umes that homologies can be determined even
I2
176
M. JOLLIE
between quite different animals (and the results reflect the beginning biases). The
‘key’ to Garstang’s approach is the idea of the common ancestry of the U-shaped
pharyngeal slit in the hemichordate and protochordate : “The common ancestor
was essentially a small stalked Ascidian with the pharynx of a young, but
symmetrical Amphioxus having only two to three pairs of U-shaped gill-slits”
(Carstang, 1928: 177). If we accept this view then the other details of pharynx
(endostyle-thyroid, epicardia-cement or adhesive glands ; and tongue barsthymus) follow as Garstang proposes. On the other hand, if the U-shaped slit in
different lines is seen as parallelism (between closely related groups) the other
pharyngeal and atrial details are not so demanding of recognition as homologues.
Filter-feeding is also a ‘loaded’ term in that it implies the homology of pharyngeal
details while losing sight of the fact that a crinoid feeds on similar organisms
without similar pharyngeal development.
Garstang (1928:53) was quite aware that “The theory just outlined imposes the
necessity of explaining the Ascidian tadpole as an interpolation in the life-history.”
This interpolation would be a solution to distribution needs and attachment site
discovery. “The author’s Auricularia theory of 1894 is therefore drawn upon to
suggest a way in which the muscular Chordate larva may have been evolved from
an original ciliated larva of the Dzpleurula type by the substitution of muscular for
ciliary means of locomotion” (Garstang, 1928:53). Important here is the idea that
this swimming larva, having acquired notochord and neural tube, is the first
chordate, derived from what must be assumed to be a hemichordate ancestor and
that it is ‘unsegmented’ in the sense that term is usually used. Garstang makes
much of this unsegmented incipient vertebrate stage.
Berrill (1955:41 -42) rejects Garstang’s idea of a relationship with
hemichordates. “I do not believe that such forms as Cephalodiscus, Rhabdopleura, and
the balanoglossids represent either separately or collectively the ancestral stock
from which the ascidian originated.” He stated (p. 40) “The more elaborate types
of echinoderm larvae, including the bipinnaria and auricularia [discussed by Fell,
19481 that figure in Garstang’s hypothesis, are highly specialized larval
adaptations for prolonging the pelagic phase of the particular echinoderm that
gives rise to them, and in no way represent primitive larval types within the
group . . . [The same is said of the tornarian, and it] is not universally present
within the Enteropneusta and probably should be regarded as an innovation that
is far from being primitive. It does not seem reasonable, therefore, to trace
evolutionary connexions along a path that leads from a highly specialized and
differentiated larval form of certain species or genera of one phylum to equally
specialized larvae restricted to only certain members of another phylum . . . This
conclusion is important in the present connexion in so far as it tends to eliminate
the echinoderm-enteropneust larval type, at least in its more elaborate [external
arms, ciliary bands, etc.] form, as the point of departure for the evolution of the
ascidian tadpole.” And (p. 36) “Apart from preconceived notions concerning
ascidian relationships . . . [withlother forms, there is every reason to regard the
typical ascidian tadpole as a unique type of larval organism evolved by the
primitive ascidian stock in response to opportunities for settling in certain
habitats.”
He thus rejects Garstang’s idea on larval development (Auricularia theory) and
insists that the tadpole larva (p. 43) “ . . . is a short-range habitat selector, not a
dispersal mechanism nor a pelagic feeder.” He continues, “The alternative to
WHAT ARE ‘CALCICHORDATA’?
177
either a concept of a gradual transformation of an echinoderm-type larva into a
tadpole larva, or the inheritance of the tadpole larva as a relic of a remote and
more highly advanced chordate past, is that it arose more or less suddenly as a
developmental innovation that had an immediate value.” He proposes that (p. 70)
“It is reasonable, therefore, to assume that potential mesenchymatous tissue
existed in the posterior region of the embryo . . . [and that] . . . the more posterior of
these cells became drawn out as passively adherent tissue [the notochord], and that
as a result of the tension so induced, myofibrillae differentiated and
contractility . . . [was] acquired. In other words, it is conceivable that, given the
initial mutation leading to chordal differentiation and extension, the tail-like
outgrowth . . . could have been supplied with lateral contractile tissue from the very
beginning.” Again the chordates appear as a larval specialization for swimming.
From such a larva i t is equally difficult to argue the further steps needed in the
development of the vertebrate.
C’riticism of the hypothejij
( 1 ) In the above, it is clear that talk of the ‘tunicate’ refers only or mainly to the
ascidians. Garstang and Berrill have much to say about the three types of tunicates
and agree that the primitive type was sessile. This sessile beginning is attested by
tunic development, presence of an endostyle (which could only have been part of
an elaborate filtering pharynx), and the opening of the gut into the atrium, a
relationship that can only be viewed as secondary. T h e tadpole larva is thus a n
indication of an earlier bilateral swimming adult retained as a motile larval stage
of a now secondarily sessile group. The origin of the Thaliacea and Larvacea is of
concern. Neotenically, the larval form was converted into the two pelagic groups :
one, the Thaliacea, has abandoned the tail for a contractile body wall (circular
bands), and the other, the Larvacea, has retained something of the larval form but
there has been great reduction of size, loss of the atrium, etc. Something of the
phylogeny of the ascidian tunicate is attested to by the marked metamorphosis that
occurs. The neotenic groups (Thaliacea and Larvacea) lack much of this,
de\reloping more directly.
(2) I agree with the advocates of the tunicate approach that the tadpole 1arj.a is a
valid stage for comparative study. I agree only in part with Grave (1944: 182-183)
who commented “TOthose who, in accordance with the Haeckelian interpretation
of the Biogenetic Law, see in the tadpole larva of ascidians the recapitulated
ancestral form of the group, failure to give ascidian larvae diagnostic systematic
value may not seem a natural and logical procedure but, to one who has become
acquainted with the profound differences in basic structures of the larval forms
characteristic of the Caesiridae, Botryllidae and Synoicedae, the conception of the
ascidian larva as a chordate ancestor seems without foundation except in the naive
wish not to relinquish any of the Haeckelian ‘facts for Darwin’. So great are the
structural differences between the larvae of species in the family Botryllidae, and
those in the family Synoicidae, that homologies in all but their fundamental
characters are sought in vain.” But of course, historically, concern has been
directed t o fundamental characters, not miscellaneous details. If the tadpole is
Lriewed as a degenerate remnant of a former adult stage, now only a larval stage, its
variation in different groups is quite understandable.
The tadpole larva of the tunicate cannot be viewed as a simple organism
transitional toward the vertebrate because it is asymmetric, headless (the mouth of
178
M. JOLLIE
the ascidian is not terminal, but dorsal), and has a large, highly evolved (complex)
pharynx associated with an atrium as a feeding structure. In the floor of the
pharynx is a well-developed, mucus-secreting endostyle, which is part of the
feeding structure, and, dorsally, a hyperpharyngeal structure of some complexity.
The tail is poorly developed and its musculature is not segmented-only a
relatively few cells are involved. The dorsal nerve tube is made up of ‘epidermal’
cells. This is certainly indicative of secondary simplification not ‘incipient
development’. Distinct larval and adult ganglia clearly indicate a highly modified
(eivolved) state.
The structure of the larva is thus a fairly direct development toward the adult
ascidian; it does not resemble an independent active state capable of giving rise to
a vertebrate. In the late 1800s, a common feeling was that the larvacean, without
tunic or atrium and with the gut opening ventrally, was a better model. ‘The
larvacean, however, is not nearly so good as amphioxus as a model of the ancestral
vertebrate, as was evident to many zoologists.
A key to the problem (decision) lies in the course and developmental e\fents of
the gut. Believers in the ascidian theory assume that the opening into the atrium is
the anus and that the tail of the tadpole is postanal. In this belief, the subnotal
strand of entoderm is either ignored or assumed to be an elongated remnant of the
neurenteric canal. The embryology of the ‘gut’ clearly indicates that the ‘intestine’
of the tunicate is the homologue of the hepatic caecum of amphioxus (or the li\rer of
the vertebrate). The so-called intestine is thus a later development and appears as
an outgrowth from the gut posterior to the stomach and below the remnant of the
cavity extending towards the tail. Such a drastic alteration of the digestive tract
speaks for a tunicate ancestor that was already attached and a filter feeder with it
complex metamorphosis; the larva was then a much reduced and altered larval
stage reflecting little of the ancestral form. Most important has been the loss of the
segmented muscles and reduction of the nerve tube to a non-nervous state.
Acceptance of this view of the gut destroys the tunicate view.
Garstang’s key argument, on the U-shaped gill slit, fits better the idea of the
ancestral tunicate as already highly modified for filter feeding. His point on the
development of the atria before the appearance of the actual pharyngeal openings
is support for such a view as is the fact that slits do not develop as such, but appear
as highly subdivided stigmata. This elimination of early ontogenetic stages says
much; yet, in the larvacean, the pharyngeal slit has secondarily returned to a
simple opening such as one would hypothesize for the ancestor of the tunicate. T h e
whole sequence, from simple slit, to one with a tongue bar or subdivided into
stigmata is seen in hemichordates and amphioxus. I prefer to view the evolution of
the modified slit as a case of independent acquisition just as I would argue that the
atria and endostyles are parallelisms (lacking in the common ancestor).
Many arguments are based on, at best, poor homologies. For example
comparison of a tunicate neural gland complex with the adenohypophysis
(anterior pituitary) assumes a greater similarity in structure than I can detect. ‘The
‘vibratile organ’ (funnel of the neural complex) may be the homologue of the preoral
ciliary organ of the enteropneust but its origin by outgrowth from the left wall of
the anterior part of the neural tube belies this. [It is said to open into the
stomodeum (Grave, 1944; Scott, 1947). Olsson (1969) found no evidence of
pituitary-like secretions in the neural gland. Another opinion is that of Komai
(1951) who suggests homology of the pituitary with the stomochord!]
WHAT :IRE: ‘C;\l.CICHORDAT.2’?
179
( 3 ) Derivation of the tunicate from a pterobranch, rejected by Berrill on other
grounds, is not possible a s the pterobranch attaches by its posterior end .while the
tunicate, like the echinoderm, attaches by its anterior end (then undergoes
metamorphosis). Thus, the pterobranch is one line of sessile animal while the
tunicate is another, and much more complex form.
The confused natrrre of Garstang’s argument is indicated by his comment
(1928 : 177) “To these characters [of the primitive ascidian] we now add that the
stalk of fixation arose \.entrally behind the endostyle, and at first contained
mesoderm only, as in Pterobranchia.” Further, Garstang was impressed with
budding in both pterobranchs and tunicates. Much of the strength of his
assumptions lay with this phenomenon.
(4)If one looks to the cephalochordate as an ancestral form (sensu lato), or a
deri\wive of ii tunicate-like animal, based on its pharynx and atrium, detailed
examination clearly shows that beyond the peripharyngeal bands the pharynx of
amphioxus has been independently evol\.ed. Independently evolved from a smaller
pharynx with simple slits and, perhaps, with only a ventral tract of cilia in place of
the endostyle.
( 5 i The position of amphioxus in this scheme is confiising. O n the one hand it can
be assumed that amphioxus retains more of the primitive features-muscle
segmentation, lanceolate shape etc.-than
the tunicate. The ‘charm’ of the
tunicate approach has been the simplicity of structure of the ascidian tadpole. This
is translated as primiti\.eness while ignoring the obvious specializations of atrium
and tunic or the interpretation of the simplicity of structure as secondary.
Amphioxrrs became then the next step toward the vertebrate or even a degenerate
vertebrate (which had lost its head). Amphioxus and the tunicate, although being
con\.ergent in some details of their pharyngeal structure, do show consistent
similarity in their early embryological stages, up to and including neurulation. In
mesoderm formation the tunicate has lost its somite development but the general
pattern is the same as in amphioxus. However, these details of their embryological
similarities ha\.e simply disappeared into the literature. Historically this similarity
was recognized by the designation ‘Acrania’ in contrast to the quite different
(embryologically) ‘Craniata’ or Vertebrata.
’Ihe tunicate hypothesis stands in strong contrast to Jefferies’ derivation of the
se\leral lines of chordates-tunicates, amphioxus and agnathous vertebrates-from
different calcichordates. The many details used Jefferies, assumed as homologues
in the contrasted groups, cannot easily be argued against for lack of real
information on the soft anatomy of calcichordates. The case against the
calcichordate hypothesis remains the “real” dissimilarity of the compared end
products. Jefferies \iews the tunicate as a “degenerate” calcichordate whereas the
tunicate hypothesis sees them as incipient chordates.
Di/)lPuroloid hvpothesis
(based on Jollie, 197.3)
‘The chordates stemmed from ii very simple metazoan, likened to the
‘dipleuruloid’ stage of the hemichordate or echinoderm; the e\.olution of the group
involved increasing size and complexity as a response to an active predatory way of
life.
180
M . JOLLIE
Development of hypothesis
(1) The tripartite body plan of the dipleuruloid links the chordates to the
hemichordates and echinoderms, an association with support from zoologists
generally. The relationship is best defined by recognizing the dipleuruloid as a
form ancestral to these several phyla; a form suggested by the larvae (and
embryology) of these present groups.
(2) Utilizing Garstang’s ( 1894) ‘auricularia theory’ the ancestral form switched
from swimming (or crawling) by cilia to swimming by undulations of the body.
This locomotor change involved segmentation of the muscle tissue. The number of
segments increased with increasing size and activity. Segments were added by
developmental subdivision of the mesoderm of the posterior body division
(metasome). Each segment was represented by a block ofmuscles on either side. A
notochord was added as an anticompression rod and as an elastic component to
improve the sinuous swimming (or creeping-depending
on the school of
thought). The dorsal nerve tube developed by invagination of a subepidermal
nerve thickening serving the largely dorsal locomotor muscles.
( 3 ) A cephalochordate-like stage was reached with a better differentiated head, a
simple pharynx with a few slits, and a large mouth. Amphioxus is thus conceived as
telling more about the origin of chordates than the tunicate.
(4) From this stage, two lines diverged. The first, in the direction of the living
acraniates, retained something of the simple early developmental stages but showed
a tendency for less activity and stronger filter feeding. Its members agreed in
having peripharyngeal ciliary bands and a ventral ‘endostylar’ band. The second,
vertebrate, line continued to increase its activity and improve its capabilities as a
predator. The head was further developed for detecting prey and directing the
swimming activity in order to seize prey.
(5) The development of the head led to the vertebrate features of paired sensory
structures (nasal, optic, otic), and a complex brain with characteristic cranial
nerves. These cranial structures clearly indicate the active nature of the animal as
does the development of gills in association with the pharyngeal slits. Thus the
ancestral vertebrate was an active, controlled swimming, predator. The
assumption that the primitive vertebrate was a filter feeder with a highly specialized
pharynx is rejected. The lamprey larva is modified in terms of filter feeding; eye,
ear and swimming control are reduced. The pharynx of the lamprey larva is not
really comparable to those of the acraniates either in form or details of function.
(6) The problem of life history should be addressed. It should be evident that the
earliest protovertebrates had a larval stage. That this stage had a pharynx used to
‘filter feed’; it had a ventral tract of cilia, which anteriorly forked as the
peripharyngeal bands. These reunited dorsally to form a dorsal tract. Food
particles were drawn through the mouth, entrapped in mucus, and carried to the
oesophagus. This pharynx differs from what we have been talking about in that it
has few and simple slits; it is not an expanded specialization for filter feeding like
that in the tunicate or cephalochordate. With increase in size, the larva switched to
predation-pursuit of and seizing prey. The important idea is that the simple
pharynx of the ancestral form is retained in the adult vertebrate where it
functioned in handling ever larger prey forms,
Style of argumentation
Something of the nature of the argumentation has already been indicated (see
also Jollie, 1973). I have assumed an early radiation of simple metazoans into
WHAT ARE ‘CALCICHORDATA’?
181
several phyla rather than deriving chordates from some already elaborated
phylum such as nemertinian, annelid, echinoderm, hemichordate or ‘non-chordate
prototunicate’. Homology is treated conservatively. The assumption that endostyle
and thyroid are homologues is not accepted. I believe that there were peripharyngeal
bands and a ventral ciliated tract in the ancestral pharynx from which highly
specialized endostyles were evolved (independently) in tunicates and
cephalochordates. Whether an endostyle as such was present in the protovertebrate
is not known. It may be that the thyroid can be traced back to a ciliated tract but
this is still not an endostyle. A ciliated tract is basically unspecialized (the whole
interior of the pharynx was ciliated). An endostyle is not seen in the pharynx of the
larval lamprey-the sub-pharyngeal gland evaginates in the floor and can be
conceived of as related to the thyroid but not necessarily an endostyle. Thus the
floor of the pharynx gave rise independently to two, somewhat different endostyles
and a ‘subpharyngeal’ gland.
I have been primarily concerned not with fine, detailed homologies such as those
of the pharynx, but with larger questions such as the origin of the notochord and
dorsal nerve tube. I have balked at Garstang’s (1928-or Berrill’s) assumption that
an epithelian nerve tube, like that seen in the ascidian larva, can be considered a
step in the direction of the functional tube of the vertebrate-rather
it is better
viewed as a deactivated remnant of what had been a functional tube-complex
structure never proceeds function! (No function is being served by the epithelial
tube that would explain its presence. I do see the possibility to produce an
invaginated nerve tube by way of the ‘Auricularia theory’.)
I am convinced that parallel developments commonly occur in closely related
lines. Garstang’s ideas on tongue-barred pharyngeal slits are better explained as
parallel developments solving (in terms of natural selection) similar functional
problems.
Embryology clearly answers some of the questions in this sort of comparative
study. For example, the ‘intestine’ of the tunicate with its opening into the left
atrium (or far forward on the body) clearly tell us that it is a modification.
‘Migration’ of the anus is not an appropriate option in terms of the observed
development. I am quite aware that development in a group of closely related
species may be variable and that its modifications may appear to tell nothing about
phylogeny-at least nothing that can be read directly from it. All developmental
\rariability, however, need not be read as revealing nothing.
Lastly, I believe in the gradual origin of new species (recognizing the reality of
sudden isolation of populations by chromosome changes or by polyploid origins).
Gradualism in my mind includes the punctuate style of Gould & Eldredge (1977).
Further, I subscribe to the view that speciation involves gene regulation primarily
(King & Wilson, 1975) and is less a matter of the ‘mutation’ approach of classical
genetics. Whereas both Berrill and Jefferies see ‘hopeful monsters’ as real
possibilities, I do not.
Criticism of the hypothesis
( 1 ) Because the tunicates and amphioxus are filter feeders and because the larva of
the lamprey feeds ‘similarly’, the ancestral vertebrate is conceived as a filterfeeding ‘agnath’ with a large pharyngeal cavity, numerous slits, and a ventral,
mucus-secreting (and endocrine) endostyle. This is a consensus view throughout
the literature. It assumes the homologies of the structural details and the
evolutionary continuity of the vertebrates with (usually) the tunicate tadpole. The
1x2
M. JOLLIE
dipleuruloid hypothesis rejects all of this. The fact that the filter-feeding structures
compared are not homologous (but independently derived in each case) does not
seem to be adequate to shake such an established opinion.
(2) T h e dipleuruloid is viewed more as a composite of assumed primitive features
than as a plan of a living organism (Clark, 1964:239). Certainly nothing like i t
(outside larval forms) is seen in the living fauna. Most thinking is done in terms of
existing groups and their larvae and efforts tend to seek the source of the chordates
(as a late group) in a living phylum. T h e fact that this morphological stage of
evolution which I have identified as a dipleuruloid is still largely retained in the
larvae of the hemichordates and echinoderms does not alter the loyalty shown to
traditional approaches. Many embryologists and zoologists, as a part of their
reaction to Haeckel’s recapitulation thinking, assume, like Libbie Hyman, that
pelagic larval forms tell us nothing. Counter views, each with some good points,
are those of Beklemishev (1969), Jiigersten (1972) or the dipleuruloid hypothesis
given here. (See Gregory’s, 1946 : 348, comments on E. B. Wilson’s course on
invertebrates.)
(3) The conversion of a tripartite organism to a multisegmented ancestral
acraniate involves a certain amount ofmagic. All of the theories are weak here as is
that of Clark (1964) for the origin of the ancestral articulate. Active swimming or
creeping appears to be the best answer for this (the chordate) change. Further the
origin of the tripartite form is not explained. I do not support a coelenterate origin
(of Remane). I do like the ideas of Valentine (1975) which suggest a functional
origin for the tripartite body design.
The dipleuruloid hypothesis has the advantage that it does not require drastic
restructuring as do the other theories, particularly that of the calcichordates. It is a valid question, how does one go from an already complex
organism to another but different form? Starting from a simple metazoan one can
go in several directions by the usually conceived evolutionary processes of
increasing morphological and functional differentiation and specialization. Thus
the dipleuruloid accounts for the chordate relationship to the Hemichordata and
Echinodermata, without requiring unbelievable restructuring, and the great
morphological differences of acraniates, tunicates and amphioxus, and vertebrates.
(4) Whereas I am proposing a gradual development of the chordate from a simple
metazoan stage rather than an existing phylum, a development in which the
cephalochordate level is seen as intermediate to the vertebrate, Gilmour
(1979: 1136) guts the whole proposition by referring to the chordate origin as from
‘fish-likeancestors’. In short, he assumes the ancestral ‘cephalochordate’ is already
of vertebrate-like complexity !
Archicoelomate theory
(taken from Gutmann, in Grzimek, 1976 and Gutmann, 1981j
A segmented, archicoelomate worm developed notochord and dorsal nerve tube
as specializations for swimming ; one line from this acraniate form developed
directly into the vertebrates, a second degenerated into the ‘trimeric’
hemichordates and echinoderms.
Development of hypothesis
(1) The archicoelomate worm was derived from a trimeric coelenterate which
arose as described by Remane. “The original archicoelomate was a worm-shaped
animal whose body has a segmental hydroskeleton, . . . [which]
., . permits
WH.2T ARE ‘C:lI.CICHORDATA’T
183
locomotion via undulating .. . movements, peristaltic-like crawling, or
burrowing . . . ” (Grzimek, 1976: 71 ; see Clark, 1964, for similar ideas).
(2) This animal took to swimming and, as an adaption for undulatory behaviour,
a notochord was formed. “The development of the notochord in the roof of the gut
can be explained by the fact that the gut is in the middle [of the body. Thus] . . . the
notochord is at the point of balance.. . [and] . . . frees the muscles . . . so they can be
used only for propulsion . . . ” (Grzimek, 1976: 78).
( 3 ) As this animal became a more effective swimmer, the anus ‘moved’ forward
from its terminal position producing a postanal tail; the coelomic pouchesjoined to
form a single body cavity. This allowed the gut to loop in the body cavity.
(4) The organism fed by taking in water anteriorly and expelling i t at the angles of
the mouth. Pharyngeal slits then arose. “This could be done by having the corners
of the mouth extend back further, but if they receded too far, the rigidity of the
flanks of the body would be threatened. Thus, some sort of transverse membranes
would have to appear, and the sides of the mouth c o d d be modified into gill
slits . . . ” (p. 79).
15) This ‘acraniate’ creature is likened to amphioxus. This type of organism then
proceeded to acquire vertebrate features such as the brain and sensory organs of
the head. “The eyes originated as optic outgrowths from the neural tube ... ”
(p. 86). Amphioxus differs from the ancestral acraniate in the development of the
pharynx, the subdivision of the slits, and the appearance of an atrium.
(6) From the ancestral acraniate, the tunicate line started by the animal spending
increased time lying on the bottom, filter feeding. Gutmann is not clear how
attachment was achieved, he merely commented (p. 70) that they “ . . . held firmly
to the floor’’ [but by which end?]. “The notochord-muscle block apparatus and
the neural tract were modified, so that the body became a sacklike structure with
an inlet for water and an outlet for filtered water. A protective layer made of
tunicin was formed on the outer surface of the body . . . ” (p. 80).
( 7 ) From the ancestral acraniate, the ‘Trimera’ arose by neoteny (Gutmann is not
clear here). The Trimera include the hemichordates and echinoderms.
[ a ) Speaking of the enteropneust, he noted (p. 81): “‘Ihey arched the fore body,
creating a space in front of the mouth. T h e muscles at the front of the body
developed and finally evolved into a proboscis-like digging structure. The stiff
notochord was a hindrance for this kind of movement, and natural selection caused
it, along with the myomeres and the neural tube, to degenerate. All that remained
were a fragment of the notochord (the stomochord) .. . and a vestige of the neural
tract. . . . The gills were moved to the hind body; . .. ”
( b )The pterobranchs and echinoderms evolved from an enteropneustlike ancestor.
“‘l‘hey also had a stomochord, a sign of their earlier chordate ancestry .. . ” (p. 82).
(c) “Echinoderm evolution occurred in the following way : pterobranchia-like
sessile species developed five tentacular rays” (p. 83). From his description the
stem of the ancestral echinoderm is equivalent to the hind body of pterobranchs.
S!de OJ argumenlntion
Gutmann emphasizes the functional approach to phylogenetic speculation
j 1966, 1969, 1976, 1981) ; that structural transitions should have a functional
explanation. I believe all of the people who have made phylogenetic speculations
would agree that an animal (species) line must be functional at all times. This view
does not mean that all the speculations will be ‘reasonable’. It should be noted that
184
M. JOLLIE
the account from which the above has been extracted is intended for the layman
and undoubtedly has suffered from translation. Samples of his statements are
included above.
Criticism of the hypothesis
(1) The primitive archicoelomate is too much like the ancestral articulate. I prefer
a more clearly separate origin for the deuterostomes (as opposed to the
protostomes) .
(2) Few zoologists (not that this is meaningful) will be willing to accept the idea
that the hemichordates and echinoderms are secondarily simplified chordates. The
comments on the stomochord totally ignore the lengthy discussions of this structure
(Newell, 1952). The assumption that the very diffuse (more so than the anatomical
accounts suggest) epidermal nervous system of the hemichordate (or echinoderm)
is derived by degeneration from the dorsal nerve tube of a chordate stands without
evidence.
(3) The argument does not cover some critical points. The dorsal nerve tube of the
chordate has always been a stumbling block to this type of argument. One needs to
know why it is there, and this theory does not ‘explain’ this. Again why are some
segmented ‘worms’ protostomes and others deuterostomes.
(4) An acraniate ancestor for the chordates (and vertebrates-likened
to
amphioxus) is an acceptable view (and has been for generations). However, the
origin of the pharyngeal slits by cutting them off from the corner of the mouth is
opposed by the general acceptance of the homology of slits in hemichordates and
chordates (which may of course be in error). Embryology also opposes this new
view, but if one is radical enough in the antirecapitulationist stance this would not
be an objection.
( 5 ) The segmentationist approach is here carried to its extreme. A segmented
coelom in the early acraniate is unlikely. I prefer to assume that only the dorsal
myotomes (and renal tubules) are segmented (associated with segmental blood
vessels and nerves).
(6) The origin of the prosome of hemichordates as a response to ‘muscular’ need is
not an appropriate ‘functional view’. Jagersten’s ( 1972) study of invertebrate
larvae clearly shows that this segment is present in almost all-it is not a new
structure but rather the original apical region of the ‘gastraea’. Development of
the prosome and its supporting stomochord suggests similar structures (purely
analogous) seen in flatworms (Ax, 1960). In the hemichordates, one sees two
distinct functions for the prosome in enteropneusts and pterobranchs. Origin of the
tail is not explained (for attachment?) but a tail lying below the anus is present in
enteropneusts.
(7) The echinoderms have a prosome in their early larval stage and they attach
(primitively) to the substrate by way of this. The adult form arises by way of
metamorphosis in which the mouth rotates toward the original posterior end of the
body. Gutmann’s comparison of the stem of an echinoderm with the ‘stem’ of a
pterobranch cannot be accepted.
(8) Gutmann’s comments on the tunicates are incomplete. Again attachment is
achieved by adhesive glands at the anterior end of what can only be conceived of as
a drastically altered larval form. It can be assumed (van Wijhe, 1927) that the
primitive acraniate had adhesive papillae for temporary attachment to the
substrate for resting (and some filter feeding?).
WHAT ARE ‘CAI,CICHORDATA’?
185
SUMMATION
These several theories, summarized in Fig. 1, differ in the package plan that they
attempt to sell. That they are speculative is at once apparent; that some of the
statements (quoted here) are reasonable must be denied. O n the positive side, the
argumentation accompanying the various proposals has had the general effect of
increasing the sophistication of thinking about them. There are two general
approaches to a problem such as this: derivation of the new group by evolution
from a simpler form, or derivation of the new group by restructuring one already,
or nearly, as complex. The first involves origin from an unknown phylogenetic
group, whereas the second utilizes a known group. Seeking origin from a known
group often involves drastic restructuring. Jefferies favours the latter while I lean
towards the former. One reason for my doing so is simple. Time is of the essence in
evolution, and the time to rebuild a group, bit by bit, is large. One might argue
that the sessile tunicate is a totally restructured cephalochordate. Simplification of
general body plan-in this case loss of nerve tube and notochord in the adult
ascidian-is not what I had in mind for restructuring. More to the point is turning
an arthropod upside down and then rebuilding it into a chordate.
Tunicote
Jeffhes
\
Echinoderm‘ hypothesis
Tunicote
+
Acroniate
Echinoderm
Q+ebrote
corpoid
Vertebrote
Tunicote
Hemichorote
Hemichordole
Echinoderm
Tunicote hypothesis
Hemichordote
Acroniote
Dipleuruloid hypothesis
/vertebr
Echinoderm
\
v
Acroni o te
Arliculoto
(Annelids, Arthropods)
Archicoelomote
Figure I . Assumed phylogenies of the several schemes described. Most of the terms are selfexplanatory. ‘Penta’ refers to five-rayed echinoderms.
I86
M. JOLLIE
‘I’he fossil record shows metazoans present in the Ediacaran (Precambrian) and
within 100 My all of the phyla (probably ) were present and largely differentiated
(Valentine, 1975). I would assume that the various lines of chordates were already
represented by soft-bodied forms early in the Cambrian (Valentine, 1975). (Highly
differentiated agnaths are now known from the Upper Cambrian.) Time is needed
for the radiation of the phylum Chordata and the only place to get it is in the
Cambrian. One might argue over how much change could be achieved in a few
million years. What we know of the fossil record does not suggest really rapid
change.
The calcichordates are well differentiated and complex organisms in the Upper
Cambrian (as are the other echinoderms and chordates). Because of the late
appearance of most of these forms (Lower Ordovician and above), it seems better
to view them as terminal types, becoming extinct in the Devonian. The affinities of
the calcichordates appear to be clearly with the echinoderms, but I would not
oppose their recognition as a subphylum.
It is evident from this account that quite different scenarios can be built around
the same facts. This in part is due to the assumed starting point. For example
Garstang assumed the ancestral chordate had tongue-barred slits whereas I have
opted for a simple slit with parallel development of tongue bars in the several lines
(including hemichordates). Gilmour (1979) is concerned about the origin of slits
and hypothesizes that they were “formed by the partial fusion of oral lamellae . . . ”
This statement contributes little to an understanding and does not account for the
position of the pair of slits of Cephalodiscus. There is little question that much
phylogenetic speculation has not been particularly well thought out or argued ;
hence Hyman’s ridicule of it.
Comparative study needs an evolutionary base and a sound base requires that
the early stages of evolution be conceived as, if not diagrammatically correct, at
least logically useful. Much current speculation clogs the system with superficial
thinking and cannot help but have deleterious overall effects on systematics. ‘I’he
fact that most proposals have little in their favour does not mean that all should be
rejected. What is needed is discussion of these to determine their strong points or
where and how they fall short. I believe that eventually a phylogeny of the
chordates built around my dipleuruloid account will be developed which will
permit us to better understand the method and course of evolution.
ACKNOWLEDGEMENTS
I want to thank Dr Dennis Kolata and Paul C. Soreno for their useful comments
on this problem and the University for both time and material support.
REFERENCES
AX, P., 1960. Die Entdeckung neuer OrganisafionrQpen im Tierreich. Wittenberg: A. Ziemsen.
BEKLEMISHEV, W. N., 1969. Principles of Comparative Anatomy of Invertebmfes, 2 vols. Chicago: University of
Chicago Press.
BERRILL, N. J., 1955. The Oritfin of Vertebrates. Oxford: Clarendon Press.
BJERRING, H . C., 1977. A contribution to structural analysis of the head of craniate animals. <oolologzco Scripfa,
6: 127-183.
CASTER, K. E., 1968. Homoimtelea. In R. C. Moore (Ed.), Treatise on Invertebrate Paleontology, pt. S,
Echinodermata I : 581 627. Lawrence, Kansas: Geological Society ofAmerica and the University of Kansas
Press.
WH;lT ARE: 'CAI,CIC:HORD.IT.4'?
187
CASI'ER. K . E.. 1971. Review of G . Ubaghs: Les kchinodermes carpoides de I'Ordovicien infkrieur de la
Montagne Noire (Francel. Journal ofPaleonfology, 4.5: 919 921.
CASIER, K . E., & E.4ION, '1'. H., J R , 1956. Microstructure of the plates in the ciirpoid echinodem
h a n a y s t i s . Journal oJPaleontolo~y,30: 61 I 614.
CI.AKR. R . H.. 1964. Qpnnrnir.\ in .2/etn:oan Eiiolution. The Origin cf the Coelom and Se.qmenk. Oxford: Clarendon
Press.
EATON, 'I. H.. 1 9 7 h . (Book review) The subphylum Ciilrichordata Uefferies, 19671,primitive fossil chordates
with echinoderm affinities. Journal oJPaleontoli!py, 44: 168.
EA'I'ON. .I. H., 1970b. The stem-tail problem and the ancestn of chordates. Journal of Paleontology, 44: 969 979.
FELL, H. B.. 1948. Echinoderm embryology and the origin of chordates. Biological Reviews of the Carnbridqe
Philosophical Soczc!,~, 2.1: 81 107.
GARSI'ANG, W., 1894. Preliininiiry note on ;I new theory of the phylogeny o f the Chordata. <oolo~gischer Anzeiger,
17: 122 12s.
GARSI'ANG, LV., 1928. T h e morphology of the Tunicata, and its bearing on the phylogeny of the Chordata.
Quarterly Journal .f Mirroscopical Science, .V.S., 72: 52 187.
GII.MOUR, T. H.J., 1979. Feeding in pterobranch hemichordates and the evolution ofgill slits. Canadianjournal
of <oulugv. 57: 1136 114'2.
GIS1.h" ' l ~ . ,1930. :llfinities hct\\ren the Echinoderm;it;i. Enteropneusta and Chordonia. <oologi.cXa Bidrag f r i n
lippsala, 12: 199 304
COULD, S.J. & I X D R E D G I ~N.,
, 1977. Punctuated equilibri;;: the tempo and mode ofevolution reconsidered.
Paleobiolop, 3: 1 15 151.
GRAVE, C.. 1944. T h e larva of Styela (Cynthia] psrtita: structure, activity and duration of life. Journal of
Morphology. 7.5: 173 190.
GREGORY, U'. K.. 1946. 'l'he roles of motile l a n a e and fixed adults in the origin of the vertebrates. Quarter!?
Reoiew of Biologv, 21: :348 364.
GL'TMANN, W. F., 1966. C~oelomgliederung,Myomerie und die Frage der Vertebraten-Antecedenten.
Z e i i x h r i j f u r <oologie, Systematik und Evolutionflorschung, 4 : 1 3 57.
GI'TMANN, W . F., 1969. Acranier und Hemichordaten, ein Seitenast der Chordaten. <oologircher Anzeiger, 182:
1 26.
GUTMANS', W. F., 1976. In B. Grzimek (Ed.], GrzimePs En<vclopedia of Evolution: 69 92. New York: van
Nostrand Reinhold.
GUI'MANN, W. F.,1981. Relationships between invertebrate phyla based on functional-mechanical analysis of
the hydrostatic skcleton. :Irnrrican CoologiJt. 21: 63 81.
HYMAN, I.., 1940 1967. The Invertebrates, vols I 6 , New York: McGraw-Hill.
J,'&ERSIEN, G., 1972. Evolution o f t h e Metazoan I . f i cycle. A Comprehensive Theoyy. New York: Academic Press.
JEFFERIES, K. P. S., 1967. Some li)ssil chordates with echinoderm aflinities. Symposia o f t h c <ooIo,~ual Society of
/.ondoti, 20: 16:{ 208.
JEFFERIES. K. P. S.. 1968. 'l'he subphylum Calcichordata Uefferies 1967)-- Primitive fossil chordates with
echinoderm afinititx Rullutin o/thu British dluspum i.\irtural Historvi, (hlogy. 16: 249 339.
JEFFERIF.S, R. P. S., 1975. Fossil evidence concerning the origin ofchordates. $yrnposia ofihe <oological Socielv of
/.ondon, 36: 253 318.
Jt:FFE:RlES. K. P. S.& 1,ELVlS. D. H., 1978. 'The English Silurian fossil PlacocvstifcsforbesinncL1 and ancestry of
the vertebrates. Philosophical Transactionr of the Royal Socie!v of I.ondon, B282: 205-323.
JOI.I.IE, M., 1973. The origin o f the chordates. Acta Zoologzca, Stockholm, 54: 81 100.
KING, hf.-C. & LVII.SON, .A. C:., 1975. F,\olution at two levels in humans and chimpanzees. Sciunce. 188:
107 116.
KOl,.A"'~\. D . K..1973. .Scalenocvstites striniplei, a new hliddle Ordovician belernnocystitid solute from Minnesota.
Journal oJ~Palrontolo.<v, 47: 969 974.
K O I A T A , D. R.. STRlhlPLE, H. L. & LEVORSON, C. O., 1977. Revision ofthe Ordovician carpoid f;unily
1owacystid;ie. Palaeontologv. 20: 529 557.
KOMAI. 'r,?1951. The homology of the notochord in pterobranchs and enteropneusts. .4merzcan .Vaturaht, 85:
270 271.
NEWEI,I+ G. E.,1952. The homology of the stomochord of the Enteropneusta. Proceedings ofthe <oological Socielv
ofl.ondon. 121: 741 746.
OLSSON, R., 1969. General review of the endocrinology of the Protochordata and Myxinoidea. General and
<,impwatiw hidiJcI~ilo/iJgY (Supplrmunt 2):485 499.
P.ACI,, C . R. C.,1977. Evolution of primitive echinoderms. In A. Hallani (Eds), Patterns ofEziolutiun: l2?J 158.
Amsterdam : Elsevier.
PHILIP, G. M., 1979. Ciirpoids-echinoderms or chordates? Biological Reviews oJthe Cambridge Philosophical Socie!v,
54: 439 471.
S C O I ' T , SISI'ER F. M., 1947. The development and history ofAmaroucium. I1 Organogenesis ofthe larval action
system. Biological Bulletin, It'oods Hole. 91: 66 RO.
CBAGHS, G . , 1967. Le genre Ceratocystis Jaekel (Echinodermata, Stylophora). (Inioersi!v of Kanras Paleontological
Contributiom. 22: I 16.
M. JOLLIE
I18
UBAGHS, G., 1968. Stylophora. In R. C. Moore (Ed.), Treatise on Inverfebrafe Paleonfology, Pt. S. Echinodermata,
I: 495- 565. Lawrence, Kansas & New York: Geological Society of America and the University of Kansas
Press.
UBAGHS, G., 1975. Early Paleozoic echinoderms. Annual Review of Earth and Planetary Science, 3: 79 98.
VALENTINE, J. W., 1975. Adaptive strategy and the origin of grades and ground-plans. American {oologist, 15:
391 -404.
VAN WIJHE, J. W., 1927. Observations on the adhesive apparatus and the function of the ilio-colon ring in the
living larva of amphioxus in the growth period. Proceedings of tht Section of Sciences, Koninklijke .Nederlandse
Akademie van Wetenschappen, 30: 991 1003.
~