AMER. ZOOL., 17:323-333 (1977).
Segmentation of the Vertebrate Head
MALCOLM T. JOLLIE
Biological Sciences, Northern Illinois University, DeKalb, Illinois, 60115
SYNOPSIS. Historical views of head segmentation are reviewed. The concensus is that the
head is segmented essentially in terms of myomeres, and that other organs have responded
in varying degrees to this. From the various lines of reasoning a model of the primitive
vertebrate is generated. This model denies the tunicate origin of the vertebrates—rather it
identifies amphioxus as most like the ancestral vertebrate. The vertebrate head is made up
of a preoral segment plus four other segments. Because of sclerotomites, the head extends
through five and a half segments. The nasal organs and eyes are preoral structures while
the ear is located between segments three and four. The occipital portion of the head
skeleton is formed from the posterior half of the fifth segment and the anterior half of the
sixth; it is vertebra-like in structure. This "segment" is much altered as a result of the
multiplication of the visceral pouches and is often viewed as the fusion product of several
segments. Thus the idea of correspondence between somite and visceral segments
posterior to the second branchial arch is rejected. In some fishes, additional vertebrae are
added to the posterior part of the cranium and this can be observed in development. The
bony cranium of the vertebrate appears to partially reflect segmentation; its components
suggest a vertebra-like developmental influence in operation. Study of the shark head has
contributed much to our knowledge of this area.
lieve that wholesale periodic reevaluations
are needed to increase the effectiveness of
The head of the vertebrate can be our effort. It is hoped that this review will
viewed as either a single entity or the stimulate a change in the "concensus" view
product of a number of segments. The of the origin of the head. It is appropriate
general concensus over much of the his- here to point out that studies of the elastory of zoological investigation has been mobranchs have been major contributors
that the vertebrate is a partially segmented to our knowledge of head segmentation.
animal and that a number of segments are
involved in the head. Just exactly what
HISTORICAL PERSPECTIVE
organs are segmented, and how, is a matter of some debate. It is the differences in
the details of interpretation that has gen- There are several reviews of head segerated the ongoing discussion and make mentation in the literature beginning with
Gaupp (1897) and continuing with Neal
this account desirable.
(1918), Goodrich (1930), Neal and Rand
This account should be more than just a (1936), deBeer (1937) and Starck (1963).
recitation of opinions or a slavish adher- The beginnings of a segmental theory are
ence to prevalent views. Generally it is held traceable to the search for a vertebrate
that science progresses by grafting new archtype based on repetition of parts
ideas to the older stems. Although this (Herder). The idea of a vertebral origin
model occasionally allows for replacement for the skull began with Goethe when, it is
of an entire limb, beliefs tend to be con- said, while walking in the old Jewish
servative and slow changing. I agree that cemetery of Venice, his attention was atmuch grafting and some partial replace- tracted to a shattered ram's skull (Fig. 1). It
ments certainly are helpful but I also be- suddenly flashed upon Goethe that the
skull, after all, might be a sort of comI want to thank Ms. Jane K. Glaser for her photo- pacted, foreshortened, anastomosed vercopy work and the Northern Illinois University for
tebral column, grown together into a
the time and facilities to do this research.
INTRODUCTION
323
324
MALCOLM T . JOLLIE
FIG. 1. Segmentation and the mammalian pattern
of bones. Dorsal series from front to back: nasal,
frontal, parietal, postparietal, supraoccipital; middle
series: orbitosphenoid, prootic, opisthotic, exoccipital; ventral series: (2, 3) basiphenoid, (4, 5) basioccipital.
helmet-like whole over the brain (Peattie,
1938:276).
Although the vertebral theory, at least in
its original form, is said to have been
destroyed by T. H. Huxley in his Croonian
lecture of 1858, a vertebral plan (Fig. 2)
was advocated by Richard Owen (1866)
and Gegenbaur (1872). Huxley, hardly a
respector of established thought, argued
that the development of the skull showed
that it was not composed of vertebrae. It
arose in a variety of vertebrates in much
the same way (Fig. 3), and formed a unit,
unsegmented chondrocranium (which is
retained in the adult of sharks and
holocephalans). Lastly its ossification
showed no similarity with those of vertebrae. This last statement is patently not true
for the occipital region (as noted by Cuvier
who saw structural similarity which he believed was due to functional similarity).
Huxley, while he argued against a vertebral theory, substituted a segmental one.
He assumed four preotic and five postotic
somites in the head. This conclusion was
based on cranial nerves and the visceral
arches. Huxley had thus shifted the direction of thought on the head about 180°
(but had not really addressed the problem
of vertebra-like cranial structure).
The real weakness of the original vertebral theory lay not with the features
Huxley discussed but in an entirely different direction, one which involved an
evolutionary approach. The theory necessitated an ancestral vertebrate with a welldeveloped, bony, vertebral column and a
minimally differentiated head. As the head
developed, the enclosing vertebral elements expanded and were extensively remodelled to accommodate the enlarged
brain, the sensory organs, and the demands of a pharyngeal skeleton. Current
belief (at least mine) does not include
much more than a supporting notochord
in the ancestral vertebrate and tacitly presumes that brain, sensory organ, and
pharyngeal development preceded significant skeletal differentiation. Therefore, vertebrae, as such, developed after
the head appeared (as stated by van Wijhe,
1889).
After a fruitless period of examination
of this question from various anatomical
approaches, developmental studies seized
upon somites as the route to understanding (Balfour, 1878; Bjerring, 1967). Although the general view is that segmentation in vertebrates is traceable to somites,
doubt has been expressed as to the occurrence of somites in the preotic region
(Kastschenko, 1888; Rabl, 1892; Froriep,
1902; deLange, 1936; Starck, 1963). If one
assumes that head somites are present,
there is then the question as to their
number (van Wijhe, 1882; Platt, 1891;
Killian, 1891; Sewertzoff, 1898; Dohrn,
1901; Gast, 1909). Further, investigation
of this problem expanded to include not
only the independent segmentation of the
body axis and the pharyngeal component
(Romer, 1972) but also such questions as
the gill slit origin of the mouth and even
the origin of vertebrates.
CIRRI OF TENTACLES
RADIAL OF FIN FOLD
FIG. 2. Segmented vertebrate skeleton, redrawn
from Owen (1866, Vol. 1)
SEGMENTATION OF VERTEBRATE HEAD
NASAL CAPSULE
LAMINA ORBITONASAL1S
.TRABECULA
OPTIC CAPSULE
POLAR CARTILAGE
.PITUITARY
OTIC CAPSULE
PARACHORDAL CARTILAGE
BODY OF FIRST VERTEBRA
NOTOCHORD
FIG. 3. Embryological beginnings of vertebrate
skull do not indicate segmentation.
In spite of the controversy, the idea of
head somites has been generally accepted;
and Matveiev (1915) identified each as
having an anterior and posterior sclerotomite (except the first). The idea of head
sclerotomites has been developed further
by Jarvik (1954) and Bjerring (1973).
DISCUSSION AND CONCLUSIONS
325
segmented musculature from which the
other evidences of segmentation have derived.
Elsewhere (Jollie, 1973), I have discussed my ideas as to the origin of the chordates and vertebrates. Clark's (1964) views
were not included and, perhaps, should be
brought in here. His analysis leads to a
phylogenetic sequence not unlike that of
other believers in the tunicate theory. In
part from Clark's ideas, I believe the ancestral oligomere was tripartite, feeding as
in enteropneusts largely by way of the
activity of the protostome. The mesosome
gave greater mobility to the prosome and
to the mouth while the metasome
functioned in burrowing—and the whole
assemblage functioned in creeping. In one
direction there were repeated origins of
sedentary lophophorate (brachiopods,
phoronids) and nonlophophorate groups
(echinoderms) and in the other modification of active feeding styles as in the
hemichordates and chordates. In this
scheme the pterobranchs are seen as secondarily reduced in size (retain remnants
of a circulatory system) and independently lophophorate — from such as the
Phoronida. The lophophore in each case is
seen as a feeding specilization not a primitive condition. The dipleurula larva is thus
more than ". . . the lowest common denominator of echinoderm and hemichordate larvae" (Clark, 1964:239).
The ancestral chordate is viewed (Jollie,
1973) as specialized for active swimming
with repeated myomeres from snout to tail
(Fig. 4). It did not have an enlarged filtering pharynx but it did have one or more
pairs of pharyngeal slits. The anus was
near the tip of the tail but there was a short
postanal tail. Associated with, and as a part
of, the locomotor mechanism was the de-
While accepting segmentation I can understand how Starck (1963) could view the
head as a unit product of developmental
pheonomena unique to vertebrates. Such a
view finds its support in many embryological facts. Such facts coupled with the obvious morphogenetic effects of the nasal
vesicle, eye, and otic vesicle seem convincing. Thus, the whole picture of development of the head as seen in reconstructions and illustrations shows no real evidence of segmentation. The evidence of
segmentation is thus largely concealed by
the derived developmental processes that
determine the ontogeny of the head—but
do not reveal its phylogeny. The whole
argument rests on acceptance of the head
cavities as remnants of the segments of the
presumed ancestral organism. However,
the argument also rests on a model of the
ancestral chordate. Only that model which
allows free (and stringent) use of known
information is acceptable and it is based on
FIG. 4. Hypothetical protovertebrate a. lateral view;
the early acquisition in chordates of a b.
anterior view showing velum closing mouth.
326
MALCOLM T. JOLLIE
velopment of the notochord and above it a
tubular nervous system serving the segmental muscles by way of segmented dorsal and ventral nerves. A head, of some
sort, with sensory organs was present. This
animal was specialized at the macrophagous end of "filter-feeding." (At this size
level macrophagy and microphagy are not
much different.)
A completely hypothetic organism such
as this does not attract attention as did the
larval tunicate following Kowalewsky's
(1866) discovery of it. Lately, the tunicate
larva has become confused with the model
proposed by Romer (1972) of a visceral
animal which acquired a somatic,
locomotor addition (Fig. 5). Romer's animal has a segmented somatic portion and
nothing is said how either notochord or
myomeres were achieved—they just happened.
As an aside here, it should be remembered that in the last half of the nineteenth
century, the question of the origin of the
chordates was one which attracted much
concern. It was in part the failure to successfully answer this question that switched
attention from comparative anatomy to
other problems.
From the ancestral chordate, in one direction, arose the living acraniates, the
tunicates and amphioxus, which live essentially sedentary lives as adults. Amphioxus
remained more like the ancestral form, but
both these groups specialized in the course
of time for filter-feeding by developing
enlarged pharynges with an endostyle and
subdivided pharyngeal slits. The beginnings of a head were lost. Since the
pharynx develops differently in the two
groups it is assumed that its form in each
arose independently. In my view the larval
tunicate is a highly modified and simplified
distributive form which has lost its segmental muscles. It has reduced the
mesoderm to a few muscle and mesen-
FIG. 5. Romer's (1972) hypothetical protovertebrate.
chyme cells, changed the course of the gut,
and expanded the pharynx in the direction of the sedentary adult. The
cephalochordate is also modified, particularly in terms of loss of the head, of the
asymmetries of the larva, the muscular
nature of the notochord (Flood, 1975)
and, perhaps, in the development of separate coelomic pouches.
From the hypothetical ancestral chordate, in another direction, stemmed the
ancestral vertebrate. This line completed
the development of the head, with elaborate paired sensory organs, along with the
appearance of other features such as the
liver, tubular kidney structure, etc. The
head was a center for search, location, and
attack on prey. The trend here was toward
increasing size, and histological complexity
of structure. Details included the adaptation of the mouth and pharynx for handling larger prey thus increasing the animal's efficiency as a predator. In this way
an entirely unique organism developed— unlike any of its invertebrate competitors. (This in itself is an explanation of
the success that the group has enjoyed.)
With this theoretical course of events in
mind let us return to the dipleuruloid state
to account for the development of that
basic chordate feature which concerns us
here, segmentation. This could involve an
increased number of coelomic cavities
added posteriorly (metamery), an increased number of somites by subdivision
dorsally of an existing space, or a combination of these.
There are two lines of explanation of an
increased number of segments. The first is
the classical view of origin from an already
segmented animal that led to wild speculations on anatomical conversion. (This kind
of speculation has involved some biologist
heroes, for example T. H. Morgan, who,
we presume through disgust, shifted to
genetics!) The second is associated with the
dipleuruloid origin—origin from an extremely simple organism. Two lines of
thought have been followed here:
Garstang (1928) visualized a tornarian-like
larva increasing in size by elongation of the
body, and shifting from ciliary to muscular
swimming. From such a beginning, seg-
SEGMENTATION OF VERTEBRATE HEAD
ment number increased by coelomic budding at the posterior end of the body. An
alternative approach assumed a creeping
dipleuruloid (Hadzi, 1963) the lateral undulatory locomotor behavior of which
would encourage selection for elongation
and segmentation. (These arguments are
rejected by Clark, 1964, who sought
primarily an explanation of metamerism
as it is seen in annelids—but something
must have preceded the annelid.)
Probably the explanation of segmentation lies with developmental details.
Romer (1972), and others, pointed out
that whatever is segmented in the vertebrate is traceable to the presence and effect
of myomeres and myomeres are traceable
to somites. Van Wijhe (1906) and Remane
(1959) suggested that in elongation the
coelomic spaces multiplied simply as a
growth device, a part of enterocoely. Van
Wijhe included the procoel and mesocoel
in the head, the latter subdividing into
four segments. (The failure of this view is
that the pharyngeal slits are metasomal in
hemichordates.) Remane's scheme has the
pro- and mesocoels- degenerating and the
somites formed from subdivision of the
metacoel along with posterior budding.
This plan, in a sense, denies all segmental
homologies between the chordates and
hemichordates. However, the presence of
a preoral lobe in the vertebrate, and the
assumed correspondence between the
premandibular head cavities and the head
cavities of amphioxus or the protosomal
cavity of the hemichordate (Goodrich,
1917) are part of the evidence suggesting
the need for modification of this view.
It is my belief that the protocoel
(axocoel) is the cavity of the premandibular segment. The mesocoel (hydrocoel) is
the cavity of the mandibular segment
which has retained its primitive association
with the mouth. The first subdivision of
the metacoel (somatocoel) is the hyoid cavity. The somites of the metocoel have appeared by a budding process with only
partial or no division of the coelom. In the
tunicate this morphogenetic process, somite formation, has been abandoned (but
the enterocoelous origin of mesoderm is
still indicated) whereas in amphioxus so-
327
mite formation has been exaggerated to
the point where each metacoelic subdivision arises separately, the coelomic portions later becoming continuous (except in
the postanal tail where the coelum is lost).
The adaptive explanation for segmentation is that it produced an efficient
mechanism for guided swimming, a necessary part of the predatory mosaic, by way
of the enterocoelic style of mesoderm production.
In my scheme the visceral arches are
usually arranged segmentally. The relationship between the first three arches (the
premandibular segment lacks an arch) and
the cranial nerves is fixed and diagnostic.
The first pharyngeal slit is between the
mandibular and hyoid arches, between the
mesosome and metasome. This position
must be a secondarily arrived at one since
in hemichordates the first slit is well back
from this margin. The fourth and succeeding arches are vagus innervated suggesting
subdivision of the nerve with addition,
posteriorly, of additional slits. Thus behind the second branchial arch there is no
correspondence between axial segments
and visceral arches (Jollie, 197 It). Variation in the number of slits then does not
require corresponding axial changes.
The mysteries of the number of hypoglossal roots and the idea of fusion or
disappearance of vertebrae—which are
not supported by observations on the
number of somites—is explainable as the
result of the morphogenetic influences of
the increase in number of pharyngeal
pouches. Once formed, the arches (exception of the mandibular) are not fixed in
axial relation but can shift backwards as in
the hagfish. This freedom from the axial
segmentation coupled with modifications
of position and development of the cranial
nerves accounts for the variation in views.
The number of hypoglossal muscle slips
and nerve roots serving them is variable;
these slips and nerves can arise further
posteriorly with expansion of the
pharyngeal region as a result, probably, of
an inductive influence.
I reject the model of a somatic addition
to an original visceral animal in which
there is no agreement between the seg-
328
MALCOLM T. JOLLIE
ments of these components. However, in
the case of the acraniates it would be futile
to argue any correspondence; in tunicates
there are no segmental nerves and in amphioxus there is a greater number of
pharyngeal slits than body segments. From
this we can conclude that pharyngeal development in each of the acraniates was
independent of the other acraniates and of
the vertebrates.
I believe that the (chordate or) vertebrate mouth is the mouth of the original
dipleuruloid which has undergone considerable modification in the evolution of
the vertebrates but has not cut back
through any premandibular arches.
(However, the mouth of the lamprey differs from that of the other vertebrates in
that the nasohypophysial complex has rotated to the top of the snout.) From this it
follows that the maxillary division of the
trigeminal is not a pretrematic branch.
The discussions relative to the cranial
nerves (Smith, 1959) are somewhat contradictory as to the pattern of each cranial
nerve, certainly the V t and V2 divisions of
the trigeminal deserve to be exceptions to
the rule. There is no good reason why the
V2 could not be viewed as a unique division
associated with the palatoquadrate which
in turn is generally viewed as the upper
limb of the mandibular arch. Romer's
(1972) discussion of cranial and spinal
nerves is accepted as clarifying the
picture — he claims that both spinal and
cranial nerves are modified from an original condition.
Assumptions that the nasal vesicle is a
remnant of a preoral gill pouch
(endodermal! — Dohrn, 1875; Marshall,
1881) or a gill cleft (ectodermal? —
Bjerring, 1972, 1973; Bertmar, 1972) have
no real substance. In my view the nasal
organs and Rathke's pouch are parts of an
original prosomal sensory and secretory
structure perhaps represented by the
"peroral ciliary organ" of the hemichordate, and Hatschek's pit (in part left head
cavity?) and wheel organ of amphioxus.
The neural gland of the tunicate appears
to be totally unrelated!
Bjerring (1973:199) goes further in
terms of segment confusion by stating
"Theoretically, this pair of [nasal] gill-slits
need not be the most anterior one. It
seems quite possible that in the deep past
of craniate evolution a pair of gill-slits, or a
median 'gill-slit,' has existed also in front
of the first metamere. . ." He suggested
that this pair of slits, or median slit, was
represented by Rathke's pouch (ectoderm)
and Seessel's pocket (endoderm). No mention is made of the original mouth.
In a more conservative vein, Jarvik
(1954) saw the effect of a premandibular
gill pouch in an assumed separation of
"epimandibular" and "epipremandibular"
components in the palatoquadrate cartilage. This interpretation could easily be
corrected by simply noting, in the development of the shark, the forward extension of the upper limb of the mandibular arch to form the whole of the
palatoquadrate. I pointed out (Jollie,
19716) that the upper end of the epimandibula is the anterior end of the
palatoquadrate which in turn is associated
with the anterior end of the trabecula and
the vertically (or medially) oriented lamina
orbitonasalis (the suprapharyngomandibular). Basic to my argument are my models
of the protochordate and protovertebrate
and observations of early developmental
stages of a number of vertebrates. Bjerring
and Jarvik's arguments lack such a base,
utilizing primarily ideas from the literature, which often are quite speculative. As
a result, Bjerring's hypothetical organism
appears to lack a mouth.
Let us examine more closely the segmentation of the axial portion of the head
'REFACIAL P1LAR <2P>
LAMINA ORBITONASALIS
FIG. 6. Diagram of vertebrate head segmentation.
Roman numerals identify cranial nerve positions;
arabic numerals identify segments; 1A-2P indicates
first (second) segment anterior (posterior) sclerotomite; P = pituitary, a = acrochordal.
329
SEGMENTATION OF VERTEBRATE HEAD
(Fig. 6). There appear to be sclerotomal
elements associated with the notochord for
each of the five and a half primary segments of the basis cranium and these appear to be vertebra-like in their development. Unfortunately our ideas of vertebral
development suffer from much confusion
(Williams, 1959; Jollie, 1962) but a few
details are generally accepted. Of relevance here is the idea that ". . . the division
of a sclerotome into cranial and caudal
parts by a sclerocoel is very probably a
primitive embryonic feature at least as far
back as the beginning of the tetrapods"
(Williams, 1959:25). This sort of thing has
been suggested for the head in fishes by
Jarvik (1972) and has been developed by
Bjerring (1973) in his considerations of the
notochordal region oiLatimeria.
Several other points call for clarification.
In my two 10 mm specimens of Squalus
acanthias (Fig. 7), Plan's vesicle lies lateral
to the anterior extension of the premandibular cavity. This vesicle arises from the
lateral surface of that vesicle and extends
directly anteriorly where it is converted
into a solid strand. There is little difference about this diverticulum other than
that it is earlier than the later outgrowths
NASAL CAPSULE
LAMINA ORBITONASALIS
PALATOOUADRATE
INFERIOR OBLIQUE
RABECULA
:YE
SUPERIOR OBLIQUE
XTERHAL RECTUS
II
INTERIOR OTIC CARTILAGE
1LA AHTOTICA
AR VESICLE
PIUA OCCIPITALIS
HEAD-VERTEBRAL COLUMN JOINT
FIRST VERTEBRA
FIG. 8. Head segmentation of shark (Squalus) as
conceived by Bertmar (1959, Fig. 43) on left and in
this account to the right. Numbers indicate segments;
P = pituitary, roman numerals identify cranial
nerve positions; verticle broken lines indicate
myotome, sclerotome white (posterior sclerotome
cross hatched on right side), notochord stippled; on
right the small circles indicate neural crest tissue, xs
indicate dermatome.
that give rise to the four rectus muscles
(Fig. 8). Bjerring (1973) points out that
tissue sheets from the Platt's vesicles of
either side meet at the midline anterior to
NERVE TUBE
Rathke's pouch. This may be true and it
may be that these cells contribute to the
GANGLION
trabecula (see Jollie, 1971a) but in any case
MANDIBULAR CAVITY
this is probably a modification peculiar to
PREMANDIBULAR CAVITY
the shark. The trabecula in most animals is
PLATT'S VES1CU
without doubt a component (pharyngo.RATHKE'S POUCH
branchial) of the mandibular arch (Jollie,
19716).
The premandibular cavities, of prosomal origin, represent the only preoral
segment in the vertebrate and it is of
interest that they connect across the midline posterior to Rathke's pouch and Seessel's pocket (Fig. 7). From this it is evident
that there has been much anterior extension of the head in the evolution of the
vertebrate, extension from the tip of the
notochord which projected into the proFIG. 7. Section (110) of 10 mm shark head (Squalus) some. Two of the sensory structures of the
showing relationship between Platt's vesicle and the head, the nasal organ and the eye are
premandibular head cavity; also relationship between
Rathke's pouch and the cross connection between the prosomal although the latter may be on
the line between segments one and two.
premandibular cavities.
330
MALCOLM T. JOLLIE
The relationship of this first segment to
the pituitary and notochord has generally
been overlooked. I believe that the acrochordal cartilage is thus of first segment
origin, not second segment origin as indicated by Bertmar (1959) and Bjerring
(1967).
A part of the problem of fitting a segmental origin to the chondrocranium has
involved accounting for the polar cartilages. Bjerring (1967) solved this problem
by deriving these cartilages from the
myotomes of second somite just as
Bertmar (1959) had derived the basiotic
laminae from the myotomes of the third
and fourth somites (Fig. 6). The observation that the polar cartilages extend anteriorly to either side of the pituitary
suggests pulling (pushing) back, and up, of
the anterior end of the notochord and
acrochordal cartilage as a part of the development of the pituitary in gnathostomes (but not agnaths).
Location of the posterior margin of the
cranium poses problems. In terms of what
has been said (about the addition of posterior pharyngeal slits and the resultant
pseudosegmentation of the occipital region), I would agree in principle with
Gegenbaur and Sagemehl that the posterior margin of the cranium is usually the
same in most vertebrates. Thus 1 have
indicated that there are basically five and
one-half segments in the head. This is
certainly the case for tetrapods and in the
earlier stages of fishes. Variations in the
number of hypoglossal foramina (2-5) are
meaningless in terms of segments. However, there is no question that vertebrae
can be added during the course of development. My observations suggest two
vertebrae are added in Squalus. These are
gradually compressed into the rear of the
neurocranium by later growth and as such
are not evident in the adult except in terms
of nerve foramina. In various bony fishes a
number of decidedly "auximetameric" additions are observed. Consider the following sequence: salmons, no vertebrae added; Esox and Polypterus, one vertebral
body added; Amia and Lepisosteus, two vertebral bodies added; and Acipenser, a large
number (undetermined). Except for
Acipenser, the neural arches remain separate, and in Lepisosteus, the two of either
side fuse into a single plate.
The most ephemeral aspect of head
segmentation is that of a relationship between cranial bones and segments and
perhaps of a vertebra-like structure for
each segment. The tetrapod (Fig. 1) seems
to present no particular problem and one
might choose to follow Williams (1959)
who restricted commentary on vertebral
development to tetrapods. However, I believe that cranial (and vertebral development) must also include fishes, recognizing
from the start the potentiality for different
and highly modified situations in various
fishes, differences that probably exceed
those between tetrapods and their presumed piscine ancestor. The problem here
is to prepare a diagram representing a fish.
I have used two, one for the sarcopterygian group and one for the actinopterygian. Both must be viewed as provisional.
Unfortunately any picture for the fish (Fig.
9) fails to show the pattern agreement one
might wish.
One should digress here to recognize
the fact that the various fish (and the
tetrapod) patterns probably condensed independently. The independent origin of
the endocrania of actinopterygian, dipnoan and amphibian are attested to by the
different positions of cranial fissures (suPOSTPARIETAL
PARIETAL
PINEAL
SUPRAOCCIPITAL
EXOCCIPITAL
"BASIOCCIPITAL
BASISPHENOID
PARIETAL
0PISTH0T1C
PTFROTIC
SPHFNOTIC
^POSTPARIETAL
SUPRAOCCIPITAL
EPIOTir
EXOCCIPITAL
BASIOCCIPITAL
ORB1TOSPHENOID
BASISPHENOID
'""OTIC
'OPISTHOTIC
FIG. 9. Two patterns of fish crania. A. Osteolepiform crossopterygian; B. Actinopterygian,
with unique bones underlined.
SEGMENTATION OF VERTEBRATE HEAD
tures) or joints in the first two and the lack
of these in the dipnoan and, probably, in
the protoamphibian (Schaeffer, 1968;
Panchen, 1964; Bjerring, 1973). The problems of bone terminology need not be
discussed here since we are concerned only
with the possibility of homologous morphogenetic, segmental or vertebra-like,
factors which could produce relatively
similar patterns.
In each of these fish figures the roof
consists of only two pairs of elements
which I prefer to identify as the parietals
(which are loosely associated with the
pineal organ) and the postparietals. The
lack of a frontal is thus characteristic of the
fishes and probably related to brain development.
The actinoptergian head skeleton poses
special problems. Patterson (1975), in an
imposing tome, challenged, among other
things, the make-up of the occipital segment. Figure 10A indicates the traditional
segment as defined by Stohr (1879); to this
I have added the extrascapular series, the
SUPRAOCCIPITAL
EXTRASCAPULAR
FORAMEN MAGNUM
EXOCCIPITAL
BASIOCCIPITAL
AORTA
CRANIAL FISSURE
(FISSURA OTICO-OCCIPITALIS)
SUPRAOCCIPITAL
INTERCALARE
EXOCCIPITAL
B
BASIOCCIPITAL
FIG. 10. Posterior view of cranium. A. vertebral
constituents; B. early teleost modified from Patterson
(1974).
331
dermal bones associated with the occipital
sensory canal innervated by the vagus.
Patterson (Fig. 10B) views the segment as
having paired dorsolateral epiotics and
paired lateral intercalars (all chondral
bones). He points out that these additional
bones are associated with the attachment
of the posttemporal bone of the pectoral
girdle to the cranium.
In either Patterson's or my scheme the
supraoccipital is seen as a neural spine
flattened and pushed into the posterior
and/or the synotic tectum. Since it does not
seem to occur in any of the "primitive"
actinopterygians (without a posttemporal
fossa), it is quite certain that the supraoccipital of the teleost and that of the tetrapods represent independent developments. In my view, the epiotics are extensions of the supraoccipital into the ear
capsule.
Anterior to the occipital segment, Patterson illustrates another (Fig. 11). This is
made up of paired pterotics and lateral
opisthotics. Ventrally, because of the
course of the cranial fissure, this segment
contributes to the basioccipital. The most
anterior segment of the "postorbital"
neurocranium, my third, has dorsolateral
sphenotics and lateroventral prootics. The
prootics form part of the basis cranii between the basioccipital and the much reduced basisphenoid.
Patterson's detailed study of these fossil
forms raises several questions as to homology and the similarity of these segments
with vertebrae. In my opinion the sphenotic and pterotic are downgrowths from
dermal bones into the otic capsule, in part
related to the support of the hyomandibula. Details aside, I am grateful that the
segmental arrangement he arrived at corresponds so well with mine. The parallel
occurrence of a basic endocranial bony
pattern (orbitosphenoid, prootic, opisthotic, exoccipital) in the various osteichthyes
suggest strongly a basic morphogenetic
system which smacks of segmentation and
vertebra-like structure.
The overall conclusion is that the vertebrate head shows evidence of mesodermal segmentation even in its chondral
and dermal bone elements. I am not
332
MALCOLM T . JOLLIE
Pto
thiforms. In P. H. Greenwood, R. S. Miles, and C.
fotc
Patterson (eds.), Interrelationships of fishes, Suppl. 1,
Epo
Zool. J. Linn. Soc. 53:179-205.
Spo
Soc
Clark, R. B. 1964. Dynamics in metazoan evolution. The
origin of the coelom and segments. Clarendon Press,
Oxford.
adf
Dohrn, A. 1875. Der Vrsprung der Wirbelthiere und das
Prinzip des Funktionswechsels. Engelmann, Leipzig.
fhm
Pro
•Boc
fotv
FIG. 11. Diagram of "primitive pholidophorid"
cranium from Patterson (1974, Fig. 118a).
suggesting that we resurrect one of the
historical accounts of a vertebral origin for
the head skeleton, but rather that a morphogenetic guidance system operating in
the head, which resembles that for vertebrae, be given more thought. It is quite
evident that much is still to be learned, yet
in the wisdom of Williams (1959:25) "descriptive detail without some guiding
theory is a mere wilderness." I hope I have
impressed you with the idea that if we can
arrive at trie right (most successful) models), we can unravel the tangled and static
strands of fact and achieve a new synthesis.
This new synthesis would tell us much
about the early evolution and biology of
vertebrates.
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