<oo&gialJwmal ofthe Linncan &xi.@ (1996), 117: 3 2 M 4 . With 31 figures
Ventilation and the origin of jawed vertebrates:
a new mouth
JON MAUAT’T
Department of<ookg~, Washington State Universi&, Asllman, WA,99164-4236, USA.
RecGiucd F e h y 1995, acc~tcdjiwfiblicndrmScptembn 1995
This study investigatesthe origin ofjaws by re-assessing homologiesbetween the oropharyngeal regions
of Agnatha and Chondrichthyes. In accordance with classical theory, jaws are interpreted as the most
anterior arches of the ventilatory branchd basket. It is proposed that jaws first enlarged for a ventilatory
function, i.e. closing the jaws prevented retlux of water through the mouth during forceful expiration.
Next, they enlarged further to grasp prey in feeding. As they enlarged, the jaws tilted forward, squeezing
the ancestral oral cavity in front of them (‘old mouth’) into a slit between the jaws and lips.
Simultaneously,the anterior part of the pharynx behind the jaws was pulled forward and became a ‘new
mouth’ (the buccal part of the buccopharyngeal cavity of gnathostomes). During the transition to
gnathostomes, the premandibular cheeks and lips of the old mouth remained in place, and are
represented in ammocoete lampreys, chimaeroids, and sharks. The stages in the evolution of
gnathostomes, driven by selection for increasing activity, are modelled as: ancestral vertebrate (with
unjointed branchial arches) to early pre-gnathostome (jointed internal arches and stronger ventilation)
to late pre-gnathostome (with mouth-closing, ventilatory ‘jaws’) to early gnathostome (feedingjaws).
01996 The Linnean Society of London
ADDITIONAL KEY WORDS:-jaws - lampreys - vertebrate palaeontology - gnathostomes
agnathans - elasmobranchs - pharynx - gills - branchial arches - holocephalians - ostracoderms.
-
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . . . . .
Material and methods . . . . . . . . . . . . . . . . . . . .
Summary of the scenario for the origin of jaws . . . . . . . . . . . .
Identifying homologies . . . . . . . . . . . . . . . . . . . .
Section 1: the pharynx . . . . . . . . . . . . . . . . . .
Section 2: jaws and pumping velum . . . . . . . . . . . . . .
Section 3 lips and mouth . . . . . . . . . . . . . . . . .
The protochordate-to-gnathostometransition: ventilation and the origin ofjaws .
Earliest vertebrate . . . . . . . . . . . . . . . . . . .
Common ancestor of all living vertebrates . . . . . . . . . . . .
Ancestor of living agnathans . . . . . . . . . . . . . . . .
Early pre-gnathostome . . . . . . . . . . . . . . . . . .
Late pre-gnathostome (ventilatory ‘jaws’) . . . . . . . . . . . .
Early gnathostome (feedingjaws) . . . . . . . . . . . . . . .
The gnathostome radiation . . . . . . . . . . . . . . . . .
Evaluation of the scenario . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . .
.
Acknowledgements . . . . . . . . . . . . . . . . . . . .
.
Note added in proof . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . .
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0 1996 The Linnean Society of London
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J. MALLA'IT
INTRODUCTION
The origin of jawed vertebrates has long interested comparative anatomists and
palaeontologists, but it has been a difficult problem to solve because the fossil record
is incomplete and because the gulf between living agnathans and gnathostomes is
perceived to be wide. Some studies suggest that the ancestors of gnathostomes had
a poorly calcified endoskeleton and were covered with only tiny scales (Denison,
1978: 12; Pearson, 1982; Reif, 1982; Schultze, 1993; Carroll, 1988; Smith & Hall,
1990: 312). That is, pre-gnathostomes were closely related to thelodonts (Stetson,
1928; Turner, 1985; Wilson & Caldwell, 1993; van der Brugghen &Janvier, 1993),
an extinct group whose whole-body fossils are so poorly preserved that they may
never yield enough information to document the evolution of jaws. Therefore, it is
necessary to construct scenarios based on living animals and the available fossils.
Development, innervation, and arteries suggest that the jaws are serially homologous
to the skeletal branchial arches behind them (Gegenbaur, 1872; Goodrich, 1930a;
Stahl, 1974: 94), and it was for a long time believed that the mandibular branchial
arch evolved into jaws to grasp prey (Gregory, 1929: 104; Lessertisseur & Robineau,
1969; 1970; Young, 1981). More recent work, however, suggests that the
evolutionary events were not so straight-forward. For example, Mallatt (1984a)
argued that the external branchial arches of known agnathans are not homologous to
the internal branchial arches of gnathostomes. Therefore, although the branchial
arches are likely the phylogenetic source for the jaws, their specific contributing
elements remain in doubt.
Like Wahlert (1970) and Reif (1982), I will argue that most changes leading to the
evolution of the grasping jaws of gnathostomes were adaptations for improved
ventilation, rather than feeding adaptations, which came slightly later. Furthermore,
when the newly evolved jaws enlarged to participate in feeding, they nearly
obliterated the ancestral mouth in front of them, leading to the formation of a new,
pharyngeal, mouth behind them.
These ideas are based on a reinterpretation of structural homologies and
hnctional comparisons between agnathans and gnathostomes, especially chondrichthyeans. Although chondrichthyeans were once thought to have evolved late,
they are now known from the Early Silurian (Smith & Hall, 1990: 313; KaratajuteTalimaa & Novitskaya, 1992), placing them among the earliest gnathostomes. Little
will be said about Osteichthyes, because I picture them as too advanced to have
much relevance for the origin ofjaws. Among the agnathans, most consideration will
be given to larval lampreys (ammocoetes), which are known to resemble
gnathostomes in such features as head segmentation, gdl structure, and arrangement
of the cephalic arteries and veins (Claydon, 1938). The analysis will follow the
phylogenetic scheme in Figure 1, which also presents other introductory information.
This paper expands and updates some previous studies (Mallatt, 1984a, b, 1985).
MATERIAL AND METHODS
Re-evaluation of jaw and mouth origins raised a number of questions about
anatomical relationships that were not answered in the literature. Therefore,
oropharyngeal structures were dissected in ten preserved dogfish Squalus acunthias,
three leopard sharks T h sem$ii.wiutus, two young Carcharhinus (species unknown),
ORIGIN OF JAWS
33 1
two hammerhead sharks Sphyrna lewini, five radish Chimaera monstrosa, and two hagfish
Eptatretus stouti, mostly from commercial suppliers (Ward's Biology, Rochester, New
York; Atchafalaya Biological Supply, Raceland, Louisiana). Surface features of other
species of sharks and chimaeroids were examined in the Field Museum of Natural
History in Chicago, as described in the text. Also examined were serial sections
through six of my own Petromyzon marinus ammocoetes that ranged from 5 to 12 cm
in body length (12 pm thick, van Gieson stain). Additionally, live Squalus acanthius and
ratfish (Hydrolagus collia) were observed at the Seattle Aquarium. Although the
I
0
'
/
\
B
/
/
-
\
\
'
4. late pre-gaathostome
3. early pre-gnathostome
2. wmmon ancestor of
all living vertebrates
1. earliest vettebrate
J. I$4ALLA'IT
332
terminology is referenced throughout the paper, Daniel's (1928) terms are used for
shark muscles.
SUMMARY OF THE SCENARIO FOR THE ORIGIN OF JAWS
To prepare the way for this re-evaluation and to place it within current views of
vertebrate origins, an overview of the scenario will be given first. The biting,
mandibular-archjaws evolved primarily through changes in ventilation. The jawless
ancestors of all living vertebrates were benthonektonic predators that ate slowmoving invertebrates Uollie, 1973, 1982a; Northcutt & Gans, 1983; Gans, 1989),
grasping their prey in a ring of oral cartilage that was squeezed by an oral sphincter
muscle. Initially, the activity level and ventilatory rate of these vertebrates were low.
The expiratory phase of their ventilatory cycle resulted from peristaltic contraction
of the pharyngeal-wall musculature, whereas inspiration resulted from the passive
recoil of unjointed internal and external branchial arches. Then, as preC
- enlargedwhenjam evolved
Figure 1. Some introductory illustrations. A, the phylogeny used in this paper. The long, almosthorizontal line at 450 million years ago indicates a rapid radiation,and is not meant to be interpreted as
an unresolved branching scheme. The relationships among the groups of jawless vertebrates are largely
from Forey & Janvier (1993), although the position of hagfish is based on Yalden (1985) and Stock &
Whitt (1992). Furthermore, galeaspids are placed tentatively with hagfish, lampreys, and anaspids,
because these groups share an enlarged premandibular oral cavity. Incidentally, the jawless
Carbonifemus fish,J5pi.rciu.r and Gi,$&tlys (Bardack & Richardson, 1977) also fit this criterion and
belong in this group. The position of conodont animals is from Peterson (1994) and that of placoderms
from Young (1986). The gnathostome phylogeny matches that in Schaeffer & Williams (1977), although
the precise relationship between acanthodians and Osteichthyes is from Pearson (1982). Below the
phylogeny are listed five stages in the evolution of gnathostomes. Stages 3-5 were probably akin to
thelodonts, whose scales, gill pouches, stomach, and pharyngeal denticles resemble those of sharks
vurner, 1985; 1991; Van der Brugghen &Janvier, 1993; Wilson & Caldwell, 1993). B, the hypothetical,
thelodont-scaled, early gnathostome. This reconstruction is based on similarities in the body shapes of
Palaeozoic sharks (Ck~&selache,Chanthus), the c h i i r o i d callmiritlchuc antarcticus, climatifonn acanthodians, and the palaeonisciiformosteichthyan W k p r r (Parker & H m d ,1962: 257; Moy-Thomas &
Miles, 1971; Denison, 1979; Pearson, 1982). C, a generalized 'vertebrate', in sagittal section, previewing
the concept of the old and new mouths, as presented in thii paper. The old mouth is stippled finely, the
new mouth coarsely.
ORIGIN OF JAWS
333
gnathostomes became more active foragers, both expiration and inspiration were
strengthened and a capacity for active, forceful inspiration evolved. Correspondingly, many new ventilatory muscles evolved and were attached to the internal
arches, which became large, jointed, and highly mobile. The most powerful of these
ventilatory muscles closed the mouth during forceful expiration to prevent leakage
(the adductor mandibulae), and opened the mouth widely during forceful inspiration
(the myotomal hypobranchial muscles); and the branchial arch on which these
powerful muscles inserted became the largest, i.e. the mandibular-arch jaws. Now,
for the first time, gnathostomes could capture evasive prey, by sucking it in through
forceful ‘inspiration’ and clamping it with bitingjaws during ‘expiration’ - the way
that living gnathostome fish feed.
The newly evolved jaws tilted and grew forward to reach the front of the snout,
a migration that reduced the premandibular oral cavity (which is large in living
agnathans: Fig. 1C) to a thin slit between the jaws and lips of gnathostomes.
However, the side walls of this ancestral oral cavity persist in living sharks as a cheeklike membrane, reinforced by a ring of oral (labial) cartilages, the supporting skeleton
of the ancestral mouth opening. Additionally, sharks have upper-lip structures that
are homologous to the large upper lips of ammocoetes, and which represent
structures used by ancestral vertebrates to probe the sediment surface for sessile prey.
In support of this interpretation, both jawed chimaeroid fish and jawless ammocoetes
retain all the lip and cheek structures associated with the ancestral oral cavity.
The above scenario will be assembled step by step, first by i d e n e n g homologies
between agnathans and Chondrichthyes and then by using these homologies to
reconstruct the common ancestor of all living vertebrates (Fig. 2). In doing this,
consideration will proceed forward from the body of the pharynx (Section 1) to the
anterior pharynx (Section 2) to the mouth and lips (Section 3). Finally, the discussion
will consider how the reconstructed ancestor evolved into known jawed (and jawless)
fish.
IDENTIFYING HOMOLOGIES
Section 1: i’?u phavnx
Constrtlctiqg the ancestral phavnx
Homohgv of lamprey and shark gilh. Living agnathans have thin, unjointed branchial
arches external to their gdls, whereas gnathostome fish have thicker, jointed internal
arches in the medial margins of their gdls. The traditional view was that these
branchial arches are homologous in both groups, meaning that the gilh of agnathans
and gnathostomes must have evolved independently from a gdl-less ancestral state
(Goodrich, 1930a: 399;Jollie, 1962: 139; 1968: 92; Moy-Thomas & Miles, 1971: 4;
Carroll, 1988: 4 1). However, Mallatt (1984a) countered this view by arguing that the
gdls of lampreys and sharks are too similar to have evolved independently: their gdl
filaments and respiratory lamellae are comparable down to the ultrastructural level,
as are their arteries (Fig. 3). The ventilatory musculature of the gdl is also similar in
both groups (Fig. 4). If lamprey and gnathostome gills are homologous, then their
respective external and internal branchial arches cannot be homologous. The
internal arches of sharks have no counterpart in lamprey gdls, but sharks have thin
J. MALLAm
334
A AMMWOETE
B
lower lips
Figure 2. Head and pharynx of an ammOcOete lamprey (A, B), sharks (C, D), and the reconstructed
common ancestor of all living vertebrates (E, F see page 336). External and mid-sagittal views. Part A
was drawn from a preserved specimen of h q k t ~ phnoi,
a
Part B from a specimen of Ic&myzonjGssm
(ammocoetesof different species are very similar in morphology). C is a schematic drawing of H@tunch
mntulntu. (redraw aRer figure 92 in Daniel, 1928). This species of shark is s h o w because it has the
primitive features of a short snout and a simple type of adductor mandibulae muscle. D was draw from
In this and all figures, numbers such as '(I)' and '(2)' are
a preserved leopard shark, T&&r scnu~iciah~~.
used to identify the ancestrallembryonicgill pouches. The ancestor may have had more gill pouches than
the eight pictured in E and F (see Arsenault & Janvier, 1991: 27).
ORIGIN OFJAWS
335
c. SHARK
first
superficial branchial
nasal
capsule
’/I
adductor
mandibulae
hyoidean interbranchid
mwcle
u
didits
hyoidean superficial
constrictor
D
internal branchial arches
336
J. MALLA?T
E.ANCESTOR
cateraal branchid arches
/
I
\
fintgill openins (“spiracle”)
b u d constrictor
QddgillOPsning
internal mandibular arch
F
I
oralvalve
byoidan h e m i i c h
sthyoidem gill pouch (2)
arch of posthyoidem
A. ADULT LAMPREY
B.AMMOCOETE LAMPREY
c. SHARK
D. A N W T O R
Figure 3. Gills of lampreys and sharks, placed around the reconstructed oropharynx of the common ancestor of all living vertebrates ( hnt a l sections). Lamprey
and shark gills are Similar, with the major components occupying the same relative positions in both gills: filaments, lamellae, septum, afferent (a) and efferent
(e) arteries, etc. The external arches of lampreys are in the same relative position as the extrabranchid cartilages of sharks, and are homologous to the latter.
An ancestral gill, based on shared features of the other gills, is reconstructed in D at lower right. All the gill pouches are numbered in the ancestral oropharpx
at centre, with '1' indicating the mandibulohyoid (spiracular)pouch.
W
W
-4
338
*
0000000
J. -‘IT
I
0
ALAMPREY
B. SHARK
Figure 4. Basic similaritiesbetween the gill muscles of lampreys and sharks (Daniel, 1928; Roberts, 1950).
In both animals, the superficial branchial constrictors (dashes)wrap around the pharynx externally and
an interbranchial muscle occupies each gill septum. These two muscles are continuous, separated only by
the external branchial arch (see Fig. 3). A straight band of muscle in the medial part of the lamprey gill
(‘median band’) corresponds to the adductor b r a n c h i of sharks.
extrubranchial cartilages in the same location as the external arches of lampreys
(Holmgren, 1946: 24; Johnels, 1948: 260; Jefferies, 1986: 159; Maisey, 1988).
As mentioned, the traditional view was that agnathan and gnathostome gills are
not homologous. The main evidence for that view is developmental, as agnathan gdls
are said to be covered by endoderm, gnathostome gills by ectoderm (Goette, 1901;
Carroll, 1988). This interpretation has been challenged and discussed at length (see
Forey, 1984; Mallatt, 1984a; Gans, 1989; Northcutt, 1990). Hence, it will only be
added that the thymus of gnathostomes, an immune organ of pharyngeal origin,
develops in the same place as the gills yet its epithelium derives from endoderm
(Daniel, 1928: 128; Fawcett, 1994: 442). This implies that the gill epithelium of
gnathostomes has an endodermal contribution, and is not entirely ectodermal as
claimed.
Given the above considerations, Mallatt (1984a) formally proposed that the gills of
lampreys and gnathostomes are homologous, but their branchial arches are not. New
evidence for this comes from three sources. (1) As M e r evidence for the
fundamental similarity between shark and lamprey gills, both contain a large venous
sinus against the gill septum, called the ‘diaphragmatic’ and ‘peribranchial’ blood
sinus, respectively (Nakao & Uchinomiya, 1978; De Vries & De Jager, 198%Tsuneki
& Koshida, 1993). In both animals, this sinus receives its blood from tiny veins that
branch off the afferent filament arteries. (2) As hrther evidence that the internal
branchial arches of sharks differ from the external arches of lampreys, these arches
lie on opposite sides of many pharyngeal landmarks in the two groups. That is, the
ventral aorta, thyroid gland, internal jugular vein, and hyoidean venous sinus all lie
ORIGIN O F JAWS
339
external to the arches of sharks, but internal to the arches of lampreys (O'Donoghue,
1914: 441; Daniel, 1934; fig. 37 in Marinelli & Strenger, 1954, 1959; Gilbert, 1973:
25; Mallatt, 1984a: 176). The extrabranchial cartilages of sharks, however, do lie
external to all these organs, exactly as the lamprey arches. For the present study, I
confirmed the above relationships in sectioned Petromyzon marinus and in dissected
Squalus acanthias. (3) As further evidence that the extrabranchial cartilages of sharks
are homologous to the branchial arches of lampreys, both of these relate to the
pericardium of the heart in the same way (Fig. 5). In adult lampreys, the pericardium
is a cartilaginous sac whose ventral part is continuous anteriorly with the
cartilaginous branchial arches. Similarly, in my dissected sharks Squalus acanthias and
Triak.issem$m&~, the ventral layer of the fibrous pericardium continues into the
fibrous membrane in which the extrabranchial cartilage are imbedded (Fig. 5B). The
hypobranchial muscles lie directly ventral to the pericardium and the external
branchial arches in both lampreys and sharks (Fig. 5C, D).
n
B
Y
-
dibmus
membranes
ventral
commissure
gill opening
\
externalarches
respiratory
/ P b
I
hypobmhhl
muscles
pericardium
extroi;ronc~d
cartilages
\
hypobranchid
IllWCIes
Figure 5. The pericardium demonstrates that the external branchial arches of lampreys (A, C) are
homologous to the extrabranchial cartilages of sharks (B, D). A and B are ventral views, showing that the
cartilaginous pericardium of lampreys connects to the external arches in the same way that the fibrous
pericardium of sharks connects to the extrabranchial cartilages (arrowheads).C and D are lateral views,
showing that the external arches of lampreys and the extrabranchid cartilages of sharks relate in the same
way to the hypobranchial muscles, pericardium, aorta and pharynx. Furthermore, the intend branchd
arches of sharks (D) have no homologue in lampreys (C).
340
J. h4ALLAl’T
7h uncestrulphutynx. If the gills and the external arches (extrabranchialcartilages) of
lampreys and sharks are homologous, then the common ancestor of these two
animals must have possessed these structures, and the pharyngeal anatomy of this
ancestor can be reconstructed. This is done in Figure 3. However, two questions
must be addressed more closely: (1) What was the ancestral arrangement of the
ventilatory muscles? (2) Were intemul branchial arches originally present?
(1) Muscles. To reconstruct the ventilatory musculature, it is necessary to compare
ventilation in ammocoetes and sharks. The following account is based on the works
of Hughes & Ballintijn (1965),Rovainen & Schieber (1975), and Mallatt (198 1). Both
ammocoetes and sharks propel ventilatory water through the pharynx unidirectionally, in through the mouth and out through the external gdl openings. Each
ventilatory cycle consists of an expiratory then an inspiratory phase. Expiration is
effected by the superficial branchial constrictor and the interbranchial muscles, the
former being a circular sheet that squeezes water through the pharynx by peristalsis
(Fig. 2A, C), the latter running in the gdl septa and acting to decrease the height of
the pharynx and compress the gill pouches (Figs 3,4). These expiratory muscles are
aided in ammocoetes by a pumping velum and in sharks by muscles to the internal
branchial arches, details of which will be provided later. During quiet ventilation,
after the expiratory muscles relax, inspiration results from a passive recoil of the
pharyngeal skeleton - recoil of the external arches in ammocoetes versus a recoil
of the extrabranchial cartilages, internal arches, and various fibroelastic membranes
in sharks. During forceful ventilation, in sharks only, inspiration is aided by the
hypobranchial ventilatory muscles, which actively enlarge the pharynx.
From the above description, it is evident that lamprey and shark ventilation share
two features: (1) expiration through the peristaltic action of superficial branchial
constrictor and interbranchial muscles; and (2) inspiration through passive recoil of
the branchial arches. Logically, that is how their common ancestor must have
ventilated, and this ancestor must have possessed the superficial constrictor and
interbranchial muscles (Fig. 3D).
(2) Infernal arches. It will be argued that the common ancestor had both internal and
external branchial arches like sharks, not just external arches like lampreys (Fig. 3D).
This conclusion is based on an out-group comparison with hagfish Holmgren (1946)
identified both internal and external arches in the anterior pharynx of Myxineglutinosu
embryos. In support of his interpretation, these embryonic arches form three sets that
relate to the eye and ear in the same way as do the first three arches of other
vertebrates (the mandibular arches lie just behind the eye, hyoid arches at the otic
capsule, and glossopharyngeal arches just behind the otic’capsule).Although these
immature arches are blastemas, they do develop into true cartilages, one set of which
remains as obviously bar-shaped in the adult hagfish as in the embryo: the ‘first
internal branchial arch’ and ‘extrabranchiale 1’ (figures 10 and 13 in Hohgren,
1946). Most impressively, Holmgren showed that all the internal embryonic arches
relate to the branchial cranial nerves in ways indicative of true arches. Although the
pharyngeal skeleton of hagfish is specialized in many other respects (Hardisty, 198l),
Holmgren’s evidence for internal arches in hagfish seems too detailed to ignore.
Based on the hagfish condition, the internal branchial arches of ancestral
vertebrates are reconstructed as unjointed and lying just below the braincase or
notochord (Fig. 2F7, as proposed previously by de Beer (1937: 4-08, 423).
Functionally, these internal arches would have helped the external arches during the
ORIGIN OF JAWS
34 1
inspiratory phase of ventilation, by recoiling along with the latter to enlarge the
pharynx and draw in water. They also may have protected the medial parts of the
gills from abrasion by prey that were swallowed through the pharynx.
As further evidence that the ancestor of living vertebrates had internal arches,
larval lampreys seem to have retained one pair of these, the intrmal velar bars
(Hardisty, 1981; “medial velar skeleton’’ of Johnels, 1948). One such bar is pictured
in Figure 2B. The ammocoete velum belongs to the mandibular region of the
pharynx, so its internal bars would correspond mostly to the palatoquadrate
cartilages (upper jaw) of gnathostomes. As predicted for a true internal arch, the
internal velar bars lie in the extreme medial margin of the velum. Further supporting
this claim for homology, they join dorsally to the trabeculae of the braincase just
posterior to the front end of the notochord (Johnels, 1948: 159), the same place
where the palatoquadrate is thought to have related to the braincase in ancestral
gnathostomes (Goodrich, 1930a: 416). In this context, it is important to point out
that the trabeculae of ammocoetes and gnathostomes are now known to be
homologous (Langdle & Hall, 1988),whereas formerly this was thought not to be so
(Schaeffer, 1975: 102; Maisey, 1986: 212).
In concluding that internal arches are primitive vertebrate characters, I must
abandon an earlier proposal (Mallatt, 1984a: 180) that such arches evolved only in
the gnathostome line when pre-gnathost mes became predators.
0
Interpretation Ofmucocartihge. The skelet n of the ammocoete velum leads to the
controversial subject of mucocartilage, whose phylogenetic significance must be
considered. Mucocartilage is not a true cartilage, but a ,flexibleskeletal tissue, present
only in ammocoete lampreys. It forms the velar bars and the entire visceral skeleton
of the head (Fig. 6). One view is that the mucocartilage skeleton evolved de novo in
ammocoetes, and has no counterpart in the cartilages of other fish or even in adult
lampreys (Johnels, 1948; Hardisty, 1979: 123;Janvier, 1933: 148).Proponents of this
view could point out that mucocartilage differs histologically from cartilage (Wright
& Youson, 1982); it transforms into true cartilages of adult lampreys only after first
rostro-dorsal
P b
Figure 6. The distribution of mumcartilage (stippling) in the skeleton of a large ammocoete. Based on
Johnels (1944)and Damas (1935).
342
J. MALLAlT
de-differentiating into a mesenchyme (Armstrong, Wright, & Youson, 1987); and
unlike the branchial cartilages, mucocartilage elements do not develop from neural
crest (Langille & Hall, 1988).
By contrast, I follow the older view that the mucocartilage skeleton is related to the
cartilaginousbranchial basket behind it, and is homologous to true cartilages in other
vertebrates (reviewed on page 270 in Johnels, 1948). There are several reasons for
such a view. First,Johnels (1948)noted that fragments of true cartilage occur within
the mucocartilage elements in the ammocoete head - and isolated bits of
mucocartilage also attach to the branchial arch cartilages - suggesting the two
tissues are more closely related than their histology indicates. Second, the
mucocartilage bar of the hyoid branchial arch, named the external hyoid bar, is an
obvious serial homologue of the true branchial arches behind it (Fig. 6): It occupies
the same relative position in the gill, just lateral to the interbranchial muscle (Fig.
15B). Third, it does not matter that the mucocartilage of ammocoetes does not
develop from neural crest, because the corresponding cartilages in the head of sharks
are not primarily from neural crest either: Jollie (197 la) saw that such cartilages in
the mouth and lip of Sqdw develop mostly fiom cells peeling off the adjacent
ectoderm, with only a lesser contribution from neural crest. Similarly, Damas (1944)
observed that the ‘ectomesoderm’ that forms the mucocartilage in embryonic
lampreys arises from nearby ectodermal ‘placodes’. I conclude that the mucocartilage elements of ammocoetes could be homologous to certain true cartilages in
gnathostomes and may contain important phylogenetic information.
This implies that in the ancestors of ammocoetes the entire oropharyngeal
skeleton was hyaline cartilage, then the anterior elements became mucocartilage
without a change in shape. This transformation would have occurred when freeswimming pre-ammocoetes became burrowers: Hardisty (198 1) interprets mucocartilage as a flexible tissue specialized to withstand the torsion generated by driving
the head through compact sand.
Evolution ofthe lumpy condition
If their ancestors had internal arches, then why did lampreys lose them? In
essence, the central lumen of the lamprey pharynx has become so tiny that the
internal arches around it became functionless and were lost. This concept is
explained in Figure 7. Still,it raises the question of why the central lumen is small.
It is small in ammocoetes to provide room for large gills that participate in suspension
feeding (Mallatt, 1981),and small in adult lampreys to provide room for the posterior
part of the lingual apparatus (‘tongue’) and a suprapharyngeal esophagus. This
esophagus is a bypass tube that lets feeding lampreys swallow blood for hours without
fouling their g d s . This line of reasoning implies that the anaspid ancestors of
lampreys lost their internal branchial arches when the adults evolved a lingual
apparatus and became continuous feeders.
Another way to conceptualize this is to point out that in adult lampreys the gdl
pouches change volume during ventilation but the central pharyngeal lumen does
not - a specialized condition (Randall, 1972). Because the lumen does not expand
and contract, no internal arches are needed for that purpose.
The velum, the other specialized ventilatory feature in lampreys, will be
considered in Section 2.
ORIGIN OFJAWS
A.ANCESTOR
343
B.ADULTLAMPFEY
Figure 7. Why internal branchial arches are not present in lampreys. These are transverse sections
through the pharynx. Part A shows the proposed ancestral condition, retained in sharks, in which external
arches surround the entire pharynx and internal arches surround the central lumen. Both sets of arches
recoiled during inspiration (arrows),thereby drawing water into the central lumen and then into the gill
pouches. Part B shows the lamprey pharynx. Here, the central lumen is so tiny that expanding it would
draw very little water into the pharynx. Therefore, internal arches would be useless, and were lost (the
original position of such internal arches is shown by the dashed circle around the central lumen).
Inspiration in lampreys is effected entirely by the external arches, which recoil to enlarge the gill pouches
(arrows in B).
Evolution of the pre-gnathostom and shark conditions
Whereas the internal branchial arches of lampreys were lost, those of pregnathostomes enlarged and became subdivided, as did the associated ventilatory
muscles. In living Chondrichthyes, the robust internal arches are divided into five
segments, connected by movable joints: pharyngo-, epi-, cerato-, hypo-, and basibranchial segments (Fig. 8). The segmentation and jointing allow muscles to attach
and pull from many different directions. Unlike the external branchial arches
(extrabranchial cartilages), which are imbedded M y in the pharyngeal wall, the
internal arches have an extraordinary range of movement within the gnathostome
pharynx. During ventilation in sharks, they are proposed to move as shown in Figure
9 (mostly after Hughes & Ballintijn, 1965, and Hughes, 1974).During expiration, to
decrease pharyngeal volume and expel water, the arch segments are flexed by
adductor branchialis and lateral interarcual muscles, and successive arches are pulled
closer by dorsal and lateral interarcual muscles (Fig. 9A). At the same time, the
lateral interarcuals swing the arches posteromedially (Fig. 9B), further decreasing
pharyngeal volume. During quiet inspiration, the bent arches recoil passively like
springs to help enlarge the pharynx and draw in water. O n the other hand, active
forceful inspiration is effected by the coracobranchial muscles, which rapidly swing
the arches anterolaterally and abduct them (Fig. 9C). At this time, the mouth is
opened widely by the coracomandibular and coracohyoid muscles (along with their
common base, the coracoarcualis). These mouth-opening muscles are sketched into
Figure 8.
Although the above-mentioned ventilatory muscles are absent from agnathans,
their phylogenetic origin may be revealed by their embryonic development in sharks.
The adductor branchialis, lateral interarcual, and coracobranchial muscles develop
from ‘branchial muscle plates’ in the gill septa (Edgeworth, 1935; Luther, 1938: 530;
Miyake, McEachran, & Hall, 1992),indicating they evolved from the interbranchial
J. MALLATT
344
i n t d arch
coracodibular muscle
cowohyoid muscle
Figure 8. Head and pharyngeal skeleton of the fiilled shark Chkzmyhsekuhus anguincur (modified from
figure 13 in Lessertisseur & Robineau, 1969). The five segments of an internal arch are labelled. The
extrabranchial cartilages are not shown. The coracomandibular and coracohyoid muscles are shown
ventrally as dashed lines.
muscles (Fig. 4). By contrast, the dorsal interarcuals, coracomandibular, and
coracohyoid muscles develop from the anterior myotomes, indicating they evolved
from epibranchial and hypobranchial myotomes, which overlie much of the
pharyngeal musculature in extant agnathans. Evidently, new, stronger ventilatory
muscles were recruited from both branchial and myotomal sources.
With the above information, the evolution of the gnathostome pharynx can be
reconstructed. In sharks, all segments of the internal arches and their associated
muscles work together as a single hnctional complex, producing strong ventilatory
forces during both expiration and inspiration. Because the structural changes
involved mere subdivision and enlargement of existing elements without extensive
migrations or rearrangement, I deduce that all parts of the biochemical unit could
have evolved rapidly and more-or-less concurrently, in response to selection for
stronger ventilation. Thus, I reconstruct pre-gnathostomes with every element
present (Fig. 10).Some authors have suggested that the earliest internal arches of pregnathostomes had only epi- and ceratobranchial segments (Jollie, 1971b; Maisey,
1980),but I reconstruct these arches with all five segments because that would make
a better spring (this agrees with Jollie, 1968; Schaeffer, 1975; and Gardiner,
1984).
I also have reconstructed the two anterior arches of pre-gnathostomes, the
mandibular and hyoid, as complete (Fig. 10) and as 111 participants in ventilation.
This follows the classical view (de Beer, 1937: 410-420; Goodrich, 1930a: 404;
Zangerl, 1981: 39), but it has become controversial and should be discussed. The
hyoid arch will be considered first. In elasmobranchs and bony fish, this arch lacks
a pharyngobranchial segment and is enlarged to support (suspend) the jaws. It has
been proposed, however, that a ‘pharyngohyal’ once existed in these gnathostomes
and became fused into the otic capsule (Jollie, 1971a). Supporting this proposal,
ORIGIN OF JAWS
345
A. EXPIRATION
muscles
\
C. INSPIRATION (FORCEFUL)
P$p
wmbranchial muscles
Figure 9. Probable movements of the internal arches during the ventilatory cycle of sharks. A, expiratory
movements, lateral view: The segments are flexed and pulled dorsally by adductor branchialis (‘ 1A’) and
lateral interarcual muscles (‘IB’), while successive arches are pulled closer together by the dorsal and
lateral interarcuals (‘2A’ and ‘2B);B, expiratory movements, dorsal view: The lateral interarcual muscles
swing the arches posteromedially(arrows);C, forceful inspiration: The coracobranchialmuscles swing the
arches anterolaterdy (large, curved mow) and abduct the arch segments (dark,diverging mows).
346
J. MALLAlT
Couly, Coltey, & Le Douarin (1993) demonstrated a small neural-crest contribution
in the otic capsule. Furthermore, in chimaeroid fishes, the hyoid arch is nonsuspensory, has a pharyngohyal segment, and resembles the branchial arches behind
it in size and shape. It has been claimed that this pharyngohyal has an odd form
flollie, 197la), but my dissections of Chinaera monstrosu indicate it resembles a typical
pharyngobranchial (see Fig. 25). Furthermore, the facial nerve descends lateral to the
chimaeroid pharyngohyal, just as the other branchial nerves relate to the
pharyngobranchials. All this suggests that the gnathostotne hyoid originated as a
typical branchial arch (Dean, 1906: 154; Patterson, 1965; Schaeffer, 1975).
The alternate view is that the chimaeroid hyoid is not primitive, but derived from
a suspensory hyoid. Maisey (1984) advocated this view, pointing out the following
ways in which the hyoid of chimaeroids differs from a branchial arch: (1) the efferent
hyoidean artery passes medial to the disputed pharyngohyal, whereas the other
efferent branchial arteries lie lateral to their pharyngobranchials (Plate 22 in de Beer,
1937);(2) dorsal interarcual muscles attach to true pharyngobranchials but not to the
chimaeroid pharyngohyal; (3) the hyoid arch lacks an adductor branchialis. To me,
these differences seem minor in light of the strong resemblance to a branchial arch.
They may simply reflect a functional need to cover and protect the efferent hyoidean
artery (which is relatively exposed) and to allow independent movement of the
chimaeroid hyoid as it directs the operculum during ventilation (the chimaeroid
operculum is discussed below). The alternate view implies that the non-suspensory
hyoid of chimaeroids resulted from the fusion of their jaw to the braincase (D.A.
EARLY PRE-GNATHOSTOME
Figure 10. The anterior skeleton and branchii muscles of a hypothetical pre-gnathostome ("early pregnathostome" of Figure 1). This reconstruction matches the verbal descriptions of Schaeffer & W i l l i s
(1977: 294) and de Beer (1937).All of the internal branchial arches are illustrated, but to avoid clutter,
only one of the Cxurnal arches is shown (the fourth).The hypobranchial segments of the arches may have
been directed anteriorly, not posteriorly as shown here (Miles, 1973); Maisey, 1989).
ORIGIN OFJAWS
347
Didier and B. Fritzsch, pers. comm.). Speaking against this, such fusion did occur in
lungfish, yet the once-suspensory hyoid of those fish did not regain the structure of a
typical branchial arch. That is, lungfish lack a pharyngohyal, their ceratohyal is
large, and the epihyal is reduced or lost (de Beer, 1937; Bartsch, 1994).
The mandibular arch of pre-gnathostomes is reconstructed as a complete ventilatory
arch (Fig. 10) for the following reasons. Jaws admittedly retain only the epibranchial
and ceratobranchial segments (palatoquadrate and Meckel’s cartilage) in all known
gnathostomes. However, in chimaeroids, the otic process of the palatoquadrate has
the appearance of a large pharyngobranchial fused to the suborbital skull (Fig. 25),
and transient hypo- and basi-branchial segments exist on the mandibular arch in
shark embryos (White, 1895; Dean, 1906: 129; El-Toubi, 1949).
Opposing my interpretation is the view that the mandibular and hyoid arches
evolved independently of the other arches, for feeding not respiration (Maisey, 1986;
1989; 1994). In support of that view, it was claimed that these two anterior arches
have no respiratory function in cyclostomes and gnathostomes (Maisey, 1989: 185).
This claim is not correct, for the hyoid arches of lampreys and primitive jawed fish
have a typical, respiratory half-gill on their posterior surface, the hyoidean
hemibranch (Jollie, 1962: 288-289). Additionally, the mandibular arch of jawed fish
bears a gdl-like pseudobranch (see Section 2). Other statements used to support the
alternate theory (Maisey, 1989) are also incorrect, i.e. that the pseudobranch is on
the hyoid arch (it is on the mandibular arch), that the facial nerve does not supply
respiratory structures (it innervates the hyoidean hemibranch), and that the first gdl
pouch of lampreys is innervated by the vagus nerve (it is innervated by the facial and
glossopharyngeal nerves, exactly like the homologous posthyoideam pouch of
gnathostomes). To be fair to the alternate view, it must be admitted that the hyoid
gdl is never entirely typical, for it lacks an anterior hemibranch and an adductor
branchialis muscle in all living fish. Still, its respiratory features are abundant enough
to argue that it evolved from a true gill; that is, the hyoid gill of elasmobranchs has
gdl-like arterial and nerve supplies, a long gdl septum with gdl rays, and typical
interbranchial and superficial constrictor muscles (Gilbert, 1973). The mandibular ‘gdl’
or pseudobranch of elasmobranchs also has such ventilatory muscles and a gdl
septum (Section 2; Fig. 16), although it lacks gill rays.
The hypobranchial ventilatory muscles of gnathostomes present special problems,
and their evolution should be considered in more depth. According to Edgeworth
(1935), the hypobranchial muscles of sharks consist of a spinal or myotomal group
(the coracomandibular, coracohyoid, and coracoarcualis), and a branchial group (the
coracobranchials), which must have had different phylogenetic origins. The spinal
group will be considered fist (Fig. 11). In ancestral vertebrates, the hypobranchial
myotomes probably lay superficial to the external branchial arches and pharyngeal
musculature (Fig. 11A, B), because this is the condition in lampreys (Marinelli &
Strenger, 1954) and hagfish (musculus rectus: Marinelli & Strenger, 1956). In
hagfish, these hypobranchial muscles run anteriorly to insert on the floor of the oral
cavity, so it seems reasonable to propose that in ancestral vertebrates they pulled
posteriorly on this floor to widen the oral cavity or open the mouth. Then, in pregnathostomes, they must have shifted to a deeper location, to insert on the
ventrolateral surfaces of the internal mandibular and hyoid arches (Fig. 11C).
Functionally, this would have allowed faster opening of the mouth through a forceful
abduction of the jaw and hyoid segments. To allow this shift in depth, however, the
c. SHARK
4
B
ORIGIN O FJAWS
349
right and left rows of external arches (extrabranchial cartilages) must have separated
from one another and moved laterally on the pharyngeal floor (Fig. 11D). As
evidence that this is possible, the two rows of external branchial arches are indeed
widely separated in ammocoete lampreys (but without any specialization of the
hypobranchial myotomes there: Hardisty, 1981: 342).
The evolution of the coracobranchial group of hypobranchial muscles can also be
reconstructed (Fig. 12). In sharks, the coracobranchials extend from the bases of the
ceratobranchial-arch segments, back along the undersurface and sides of the fibrous
pericardium to the coracoid bar of the pectoral girdle. Because these are branchial
muscles, they must be homologous to the ventral part of the interbranchial muscles
in lampreys. The latter attach to the ventral commissure of the external branchial
coracobranchial
muscle
l
id
A. PRE-GNATHOSTOME
B. GNATHOSTOME
Figure 12. The coracobranchialgroup of hypobranchial muscles. A, the coracobranchialsevolved from
the ventral part of the interbranchial muscles and initially attached only to the fibrous pericardium; B,
this pericardial attachment then moved posteriorly to reach the coracoid bar of the pectoral girdle. T h e
small picture of the shark above provides orientation.
Figure 11. The spinal group of hypobranchial muscles. These ventilatory muscles of gnathostomes
evolved from locomotory myotomes. A, Ventral view of a lamprey (based on a dissected Petrmyzon marinllr
and on figure 16 in Marinelli & Strenger, 1954). The hypobranchial myotomes have been cut away from
the lamprey’s left side, exposing the external branchial arches and the superficial branchial constrictors;
B, transverse section through the floor of the lamprey pharynx, showing the relationship between the
hypobranchial myotomes and the external arches; C, ventral view of a shark (based on dissections of
Squalus acanthinr)).The hypobranchial muscles - coracomandibular,coracohyoid, and coracoarcualii
lie much deeper than in lampreys and are concentrated near the ventral midlime. For superficial
myotomes to have migrated so deeply, the right and left sets of extrabranchial cartilages (external arches)
must have moved apart. Later, the first two interbranchial and superficial constrictor muscles, which
originally had a lateral location, must have grown ventro-medially until they covered the hypobranchial
muscles (see the dark arrow in the intermandibular muscle); D, transverse section through the floor of the
shark pharynx, showing the right/left separation of the extrabranchial cartilages and the deep location
of the coracomandibular and coracohyoid muscles. Notice that the right and left cartilages remain
interconnected across the midline by the fibrous pericardium (dashed h e ) . This means that the
hypobranchial muscles did not migrate through any tissue layers when they sank to their deeper
location.
~
350
J. MALLATI‘
arches in the midline (Fig. 4A), which is continuous with the pericardium (Roberts,
1950). This fact implies that the coracobranchials of pre-gnathostomes attached to
the fibrous pericardium (Fig. 12A), and indeed, in shark embryos, the ventral ends of
these muscles develop from the pericardial wall (Edgeworth, 1935: 154). Additionally, my dissections of adult Squulus acunthias show that the anterior coracobranchials
are heavily fused to the caudal part of the fibrous pericardium, using thickenings of
the latter as aponeuroses to insert onto the coracoid (dashed lines in Fig. 12B).
Marion (1905) made a similar observation. These facts suggest that during the
evolution of gnathostomes, the attachment of the coracobranchials moved
posteriorly along the pericardium until it reached the coracoid. Importantly, the
intermediate stages in such an evolutionary sequence would make functional sense:
Posterior attachment to a strong, fibrous pericardium would allow the coracobranchials to pull back on and flare the branchial arches almost as effectively as would a
coracoid attachment. The coracoid merely represents a more massive anchor.
Outgroup comparison
This section considers how well the pharynxes and ventilation of other vertebrate
groups fit my model of the ancestral condition.
Chimwods. Starting with gnathostomes, among the cartilaginous fishes, chimaeroids
have certain specializations not seen in sharks (see Fig. 25). The gill septum of the
hyoid arch, along with the associated hyoidean interbranchial and superficial
constrictor muscles, extend far posteriorly to form a soft ‘operculum’, which is
supported by an opercular cartilage (Goodrich, 1930a: 498; Edgeworth, 1935; Stahl,
1967). Because of this opercular cover, only one external gdl slit exists per side,
compared to five or more in sharks and ancestral gnathostomes (Goodrich, 1930a:
486; Miles, 1973). Muscles that run to the opercular cartilage and hyoid arch
presumably pull these elements forward to increase pharyngeal volume during
inspiration (i.e. the interhyoideus and, perhaps, levator hyomandibulae muscles:
Edgeworth, 1935: 97).
Functionally-similar but bone-containing opercula evolved independently in the
acanthodian/osteichthyan line and in placoderms (Young, 1986). Such a high degree
of parallel evolution is not surprising when it is considered that opercula provide two
widely beneficial functions: strengthening the maximum force of the inspiratory
pump, and allowing this pump to exert a constant suction pressure throughout each
inspiratory period (Alexander, 1978: 84). One might ask why all opercula evolved on
the hyoidean gdl, as opposed to some other. It may simply reflect a derivation from a
shark-like condition, where the hyoidean interbranchial and superficial constrictor
are the largest and strongest of all expiratory muscles (Fig. 2C). Functionally, if any
ancestral ventilatory muscle is to be enlarged to increase ventilatory strength,
efficiency demands that it be the anterior, hyoidean muscle, because only this pumps
all the ventilatory water (i.e. the more posterior constrictors pump successively less
water because water leaves through the gill slits).
In chimaeroids, all superficial constrictors posterior to the hyoidean have been
lost, presumably because the operculum took over their expiratory function (or
alternatively, because enlarging shoulder muscles pushed onto the posterior pharynx
when chimaeroids began to s w i m by flapping their pectoral fins). The first superficial
constrictor of chimaeroids, associated with the mandibular arch, was also lost. This
may have occurred when the jaws fused to the braincase, prohibiting the adduction
ORIGIN OF JAWS
35 1
of the right and left jaw rami that this mandibular constrictor provides in other fish
(i.e. the intermandibularis muscle: Lauder, 1980b).
Although the superficial constrictors of chimaeroids are highly modified, most of
their other branchial muscles resemble those of elasmobranchs (adductors,
interbranchials, and dorsal interarcuals: Edgeworth, 1935). The hypobranchial
muscles are extremely simple, lacking a coracoarcualis (Jollie, 1982b). The gdls
themselves are structured like elasmobranch gills, except the lateral parts of the septa
are reduced in length (Goodrich, 1930: 498). This reduction reflects the loss of the
parabranchial chambers, the components of the inspiratory suction pump whose
function was taken over by the operculum (Hughes, 1974).
Adult lampreys. Turning to agnathans, the pharynx of adult lampreys is specialized for
tidal ventilation, in which the gdl pouches do all the pumping, and water is both
inspired and expired through the external gdl openings (Roberts, 1950; Randall,
1972; Rovainen, 1982). Despite this unusual ventilatory pattern, the gills and
branchial muscles of adult lampreys seem relatively unmodified (Figs. 3, 4). The few
structural specializationsin their pharynx include complex valves on the external gdl
openings that direct the tidal flow, and the division of the ancestral pharynx into an
oesophagus and a respiratory pharynx (see above).
Hagfish. Hagfish have perhaps the most highly modified pharynx and gdls of any fish
group. The anterior three gill pouches, starting with the mandibulohyoid pouch, are
lost during development (Stockard, 1906),perhaps to make room for the expanded,
pumping velum. The remaining gills migrate far posteriorly, perhaps to prevent
exhaled water from fouling the inspiratory water in the sediments inhabited by these
burrowing animals (Johansen & Strahan, 1963).The external branchial arches of the
gdls are reduced to tiny rings in the walls of the exhalent ducts, and internal arches
are absent from the gdls. This reduction of the pharynx-expanding branchial arches
reflects the fact (personal observation) that the hagfish pharynx does not pulsate
during ventilation but retains a constant diameter - presumably because gross
pharyngeal movements would be resisted by the packed sediment in which the
hagfish live and would exhaust the animals. Hagfish gills have an unusual pouched
form and an arrangement of branchial arteries that differs from that in all other fish
(Mallatt, 1984a). Mallatt & Paulsen (1986: 176) considered hagfish gdls to be highly
derived structures, secondarily modified for life in the anoxic muds of the deep-ocean
floor.
Ostracodm. Whereas the pharynxes of chimaeroids and hagfish are modified, those
of fossil agnathans (ostracoderms)seem much like that of the reconstructed ancester
(Fig. 13). Among the ostracoderms, the heterostracans, osteostracans, and galeaspids
are known well enough to permit identification of the ventilatory structures. In these
groups, the gdl pouches formed simple, repeating impressions on the bony head
shields. In interpreting the specific pouches and intervening arches, several rules
were followed. (1) I began with the general rule that the arch directly behind the eye
is the mandibular arch; that the gdl pouch between the eye and otic capsule is the
first (mandibulohyoidor spiracular) pouch; and that the hyoid arch lies at (or slightly
anterior to) the otic capsule. This is the usual arrangement in vertebrate embryos,
including embryonic hagfish, lampreys, elasmobranchs, and the chimaeroid
Callorhinchus (Pasteels, 1958; Edgeworth, 1935; Forey, 1984: 339; Jefferies, 1986:
Chapter 6: Larsen, 1993); and it is retained in ammocoetes and adult sharks. This
352
C
ORIGIN OF JAWS
353
must be the primitive vertebrate arrangement because the nerves associated with the
mandibular and hyoid arches (trigeminal and facial) always leave the skull behind the
eye and anterior to the otic capsule, respectively. When applied to the fossils, the rule
generates Stensio's (1958) interpretation of the heterostracan pharynx (Fig. 13A). (2)
The osteostracans are an obvious and rare exception to Rule 1, as their pharynx had
shifted far forward relative to the eyes and otic capsule (Fig. 13B). In this group, I
identified the mandibulohyoid and posthyoidean gJl pouches as containing the endbranches of the facial MI) and glossopharyngeal (IX) nerves, respectively (with the
facial nerve identified by its association with the acoustic nerve, and the
glossopharyngeal identified at the posterior part of the otic capsule, near the brain:
Janvier, 1985). This generated the same reconstruction of the osteostracan pharynx
as provided by Allis (1931), Lindstrom (1949),Jollie (1962)) and Moy-Thomas &
Miles (1971: 16). (3) Galeaspids fit Rule 1 in that their first gill pouch generally lies
just behind the eye (Forey, 1984: 339). Their trigeminal and facial nerve canals
cannot be traced far, but seem to run toward the first and second gill, respectively
(Fig. 13C; also see Plates 3 and 4A in Wang, 1991).
All the above-named ostracoderms had extenzal branchial arches (Janvier & Blieck,
1979; Janvier, 1981; 1984), and the present model predicts that unjointed,
uncalcified intemal arches were also present but did not fossilize. Superficial branchial
constrictor muscles probably were absent (as the gill pouches touch the superficial
bony shields), but interbranchial ventilatory muscles could have been present
(Watson, 1954: 5). The fossils show parabranchial chambers lateral to the gJls (Forey,
1984: 338). These water chambers also exist in ammocoetes and sharks (Fig. 3),
where they comprise a 'suction pump' that pulls water across the gills during the
inspiratory phase of each ventilatory cycle (Hughes, 1974; Mallatt, 1981: 1 12). Other
aspects of the ventilatory mechanisms in these ostracoderms wiU be considered in
Section 2 on the velum.
Amphioxus. Ventilation in the protochordate amphioxus, and its relation to that of the
earliest vertebrates, are discussed by Gans (1989: 238-243). I have nothing to add to
that scenario, but should note that it involved a switch from ciliary to muscle-driven
ventilation, as the branchial bars changed from suspension-feeding elements to
respiratory structures with gills.
Section 2: Jaws and pumping velum
This section focuses on the most anterior part of the pharynx, the region that
relates most closely to the origin of jaws.
Figure 13. Oropharyngeal structures of ostracoderms. A, Heterostracan: Impression of the pharyngeal
k of Stensio, after figure 197A in Stensio, 1958); B, Osteostracan:
roof of Prcrarpis (Sim0pteruspi.sp
Spatuhfir species (redrawn from figures 90 and 91 inJanvier, 1985); C, Galeaspid DupnaSpirpaovMgmrir
(redrawn from figure 3 in Halstead, 1979); D, Thelodont: lUriniapogn'(from figure 186 in Stensio, 1958,
and photos supplied by Susan Turner).My identification of structures is based on the assumption that the
mandibulohyoid pouch is the pouch directly behind the eye (A, C, D) or is the pouch supplied by the
facial nerve (B). Because all the ostracoderms pictured had an unaltered mandibulohyoid pouch, they
must have lacked a velum. V = trigeminal nerve (maxillary and mandibular branches); Vn = facial
nerve; IX = glossopharyngealnerve; X, = first branchial branch of the vagus nerve.
354
J. MALLATT
Conrtmctirg the ancestral condition
Ammocoetes. As shown in Figure 2B, the main structures in the anterior pharynx of
larval lampreys are: (a) the pumping velum; (b) the pocket or space behind the velum;
(c) the hyoidean hemibranch; (d) the first permanent gill pouch; and (e) the first
complete (posthyoidean) gill.
The velum is a pair of cupped, muscular paddles that push water posteriorly into
the pharynx during the expiratory phase of each ventilatory cycle. It is a powerful,
piston-like pump that can work against back pressure (Rovainen & Schieber, 1975)
and force ventilatory water through the sand in which ammocoetes live. Projecting
posteriorly from each velar paddle is a mdkljap, which is supported by the internal
velar bar (Fig. 2B). When the velum starts to contract, its right and left medial flaps
come together to form a seal that prevents reflux of water from the pharynx through
the mouth (Homma, 1975). In the embryonic lamprey, the velum develops at the
border between the mouth and pharynx, from the buccopharyngeal membrane
(Claydon, 1938). Its muscles belong to the mandibular branchial segment, being
innervated by the mandibular branch (V,) of the trigeminal nerve (Hardisty &
Rovainen, 1982;Jefferies, 1986).
The pocket behind each velar paddle represents the first (spiracular or
mandibulohyoid)gill pouch of the embryo (Sterba, 1953: 249-253). In lampreys, the
w d s of this pocket bear no gills, and there is no opening to the exterior (no
spiracle).
The hyoidean hemibranch contains only posterior gill filaments. A ciliated
pseudobranchkl groove, associated with suspension feeding, runs vertically along its
medial margin (Mallatt, 1979; 1981). Posterior to the hemibranch lies the first
permanent gill pouch and the first complete (posthyoidean) gill. The latter consists of
an anterior and a posterior hemibranch.
Elasmobranch. The corresponding structures in the anterior part of the elasmobranch
pharynx are (Fig. 2D): (a) jaws and oral valve; (b) spiracular pouch; (c) hyoidean
hemibranch; (d) first typical gill pouch; and (e) first complete (posthyoidean) gill.
As mentioned, the jaws of gnathostomes are internal mandibular branchial arches,
homologous to the internal velar bars of ammocoetes. The oral ualues of
Chondrichthyes (Fig. 14) have received little attention in the literature, but my
dissections reveal that they attach to the posterior surfaces of the palatoquadrate and
Meckel’s cartilage in the same way the medial velar flaps attach to the internal velar
bar in ammocoetes - and they likewise shut to prevent reflux of expiratory water
through the mouth (Hughes, 1974: 22; Dean, 1906: 18).It is possible that the oral
valve is the remains of the embryonic buccopharyngeal membrane, because the
latter also lies directly posterior to the mandibular arch in gnathostomes ( h e y , 1974:
2 14; Alluchon-Gerard, 1976: 123; Waterman & Schoenwolf, 1980: 442). Given these
considerations, I propose that the oral valves of cartilaginous fish are homologous to
the medial velar flaps of ammocoetes.
Posterior and dorsal to the jaws of elasmobranchs lies the spiracular pouch (Fig.
2D), which develops from the first embryonic gdl pouch. It opens to the exterior at
a spiracle (Fig. 2C), a hole through which water is inspired (not expired, as through
the other gill slits: Hughes, 1974). The anterior wall of the spiracular pouch contains
a gdl-like pseudobranch (Goodrich, 1930a: 5 19), whose function is incompletely
understood. It is not respiratory, for it receives only oxygenated blood. Laurent &
Dunel-Erb (1984) concluded that the pseudobranch senses the chemistry of blood
ORIGIN OFJAWS
355
that has just flown past the inspiratory water entering the pharynx. If this exposure
to ventilatory water has changed or disrupted the blood chemistry, the pseudobranch
secretes hormones that correct the disruption. It might also sense the chemistry of the
water directly. In this way, the pseudobranch would allow fish to adjust to hypoxic,
acidic, or polluted water.
Despite its non-respiratory function, the pseudobranch probably evolved from a
typical respiratory gdl (Laurent and Dunel-Erb, 1984: 305; Romer, 1970: 3 10). Like
a gdl, it has filaments and lamellae plus a diagnostic gill vessel called a cavernous
body. The arrangement of the small arteries in its filaments and the early
development of its main artery are like that of the other gdls.
Although the spiracular pouch has a dorsal location, a blind pocket lies ventral to
it in some sharks, between the hyoid arch and the lower jaw (‘blind pocket’, Fig. 2D).
This pocket may represent the ventral half of the ancestral mandibulohyoid gdl
pouch (Smith, 1937: 429).
Farther posteriorly, elasmobranchs and primitive bony fish have a hyoidean
hemibranch (Jollie, 1962: 287-289). It corresponds to that of ammocoetes, although
there is no pseudobranchial groove on the medial surface of the internal hyoid arch.
Behind that, the first typical gd pouch and first complete gi€l resemble those of
ammocoetes.
The ancestral condition. To summarize the main differences between the anterior
oral valve,
dorsal flap
oral valve,
B.CHIMAWA
Figure 14. Oral valves of Chondrichthyes. These valves lie directly behind the jaws and teeth. A, the open
mouth of a skate Raja (R. ninacea?)contains an especially obvious oral valve, composed of both dorsal and
ventral flaps. The sagittal section below shows how the valve flap attaches to the extreme posterior point
of the jaw cartilage; B, Chimaera momtrosa, with the right half of its lower jaw pulled forward to reveal the
oral valve just behind it (this is the ventral flap; a dorsal Rap lies medial to each posterior upper tooth plate
and is not shown). Sectioned material indicates that the oral valves of Chondrichthyes contain no muscle,
so they must close passively. Sharks are not included in this figure but their oral valves are pictured
elsewhere: Those of Tri~kzisemfh.rciuhu are in Figure 2D, and the blunt, hctionless valves of Sgunlus
acanthicrr are in Figure 31D. I also saw oral valves in specimens ofNoobrhynchuc macuka&~~,
q h p a lewini, and
Clamydosehhtu a n g u k (Gudger & Smith, 1933: 269); and they were especially large in Hctcrodonhrs
japonica and Gingvlosroma & a h .
356
J. h4ALLATT
pharynxes of ammocoetes and sharks, only ammocoetes have a pumping velum
whereas only sharks have filaments and a gill pouch behind the mandibular arch (the
pseudobranch and spiracular pouch). I will argue that the common ancestor of these
animals was closer to sharks in these respects. Forey &Janvier (1993; 1994)proposed
that this ancestor had a pumping velum, which later gave rise to the jaws of
gnathostomes, but it is here concluded that no velum was present. The evidence for
this conclusion comes form ostracoderms. First, the oral cavities of both
osteostracans and heterostracans are too small to have housed a large velum (see Figs
13B and 28A). To illustrate this,the velum chamber of ammocoetes and hagfish is
larger than two gill pouches, yet the corresponding oral cavity of most osteostracans
is smaller than any single gdl pouch (Fig. 13B). Second, a large velum forming the
anterior border of the mandibulohyoid pouch would have affected the size and shape
of this pouch - yet this pouch in the ostracoderms is not enlarged and it looks
exactly like the other gill pouches behind it (Fig. 13), and can bear impressions of
branchial muscles or gdl filaments. The mandibular filaments of ostracoderms may
have formed either a pseudobranch or a respiratory gdl, but such filaments could not
have functioned on the back of a vigorously pumping velum, which would jam them
together and prohibit respiratory exchange. I conclude that a large, pumping velum
was absent from the ostracoderms in Figure 13 and is confined to ammocoetes and
hagfish, helping these burrowers to force ventilatory water through the pharynx and
impermeable sediment.
Based on these comparisons and functional arguments, the anterior pharynx of the
common ancestor of all living vertebrates is reconstructed in Figure 15A. The
reasons for including a mandibulohyoid gill pouch were just given; and the oral
valve, internal mandibular arch, and hyoid hemibranch are all common to sharks
and ammocoetes. The external mandibular arch is based on the external velar bar
of ammocoetes (Fig. 6), and it may be represented in elasmobranchs by spiracular
cartilages (Ridewood, 1895; Edgeworth, 1935: 34), which occupy the expected
position anterior to the spiracle (but see El-Toubi, 1947, for a different interpretation
of spiracular cartilages). The musculature of the ancestral mandibular gill is assumed
to have been like that of the other gills because an interbranchial muscle and a
superficial branchial constrictor are associated with this arch in sharks (i.e., levator
maxillae, first dorsal constrictor, and first ventral constrictor [intermandibularis] of
Daniel, 1928: 85).
Evolution of ,h?
ammocoete condition
If the pumping velum is not a primitive character, from what structure did it
evolve? One might guess it is a modified version of the mandibular gdl, but evidence
indicates it is more than this (Fig. 15B). The ammocoete velum contains distinctive,
‘tubular’ muscle fibers (Hardisty & Rovainen, 1982). In more posterior parts of the
ammocoete pharynx, tubular muscles are confined to the lateral wall, as part of the
superficial branchial constrictors (Alcock, 1898). This suggests that the first
(mandibular) constrictor migrated into the mandibular hemibranch from the lateral
pharyngeal wall (Fig. 15C). By rotating into the transverse plane, this muscle could
push water straight posteriorly, greatly increasing the force of the ventilatory pressure
pump. In support of this interpretation, a recent gene-labelling study (Holland et al.,
1993) indicates that the largest pumping muscle in the ammocoete velum
(velothyroideus)is homologous to the superficial constrictors of the mandibular arch
in a teleost fish (levator arcus palatini, dilator operculi). Other facts support such a
ORIGIN OF JAWS
A. ANCESTOR
357
B. AMMOCOETE LAMPREY
C. PRE-AMMOCOETE
Figure 15. Evolution of the most anterior part of the pharynx: ancestral and ammocoete conditions. As
in the other figures, gill pouches are numbered (1 and 2) according to the ancestral scheme. A, proposed
ancestor of all living vertebrates, f r o n d section (for orientation, see the inset at upper left). An uncertain
part of the reconstruction is the anterior hemibranch in the hyoid gill, for this is absent in all living
vertebrates, embryonic and adult. However, the complete nature of the mandibulohyoid gill pouch in
heterostracans and osteostracans may mean that an anterior hyoid hemibranch once existed; B,
ammocoete. Here, a muscular, pumping velum resulted when the first superficial branchd constrictor
migrated mediaUy into the mandibular gill (dark arrow), with a consequent loss of the mandibular gill
filamentsand the fimt gill opening. As evidence for such a derivation, distinctivetubular muscle fibres that
occupy the pharyngeal wall are also present in the velum. The ancestral oral valve became the medial flap
of the velum; C, This lateral view reiterates the theory that the first superficial branchial constrictor
moved anteromedially to enter the ammocoete velum.
J. MALL4lT
358
homology: (1) the main velar muscles develop as part of the superficial constrictor
series in embryonic lampreys (‘constrictor veli’ in fig. 423 in Luther, 1938); (2) my
serial sections of ammocoetes show that the superior part of another velar muscle,
velohyoideus, lies between the external velar bar anteriorly and the external hyoid
bar posteriorly (i.e. between the first and second external branchial arches), which
matches the expected location of the fist superficial constrictor in ancestral
vertebrates (Fig. 2E).
When a velum evolved in ammocoete ancestors, the first external gill opening
behind it was lost, possibly to keep its branchial valve from leaking under the
pressures produced by the velum.
A
EARLY PRE-GNATHOSTOME
B. LATE PREGNATHOSTOME
dargal epimandibular
of mandibular arch
\
S b uceratomandibular
h arch
C. EARLY GNATHOSTOME
D. SHARK
jaw
oOnctriCt0r
mlJ3cie
bUlariS)
lost hsrs
ORIGIN OF JAWS
359
Evolution of the pre-gnathostome and shark conditions
The above considerations seem to argue against the hypothesis of Forey and
Janvier (1993; 1994) that the jaws of gnathostomes evolved from a velum. That
hypothesis, it seems, would have to explain the homology between the velothyroideus
muscle of ammocoetes and the first superficial constrictor of gnathostomes in terms
of the former muscle giving rise to the latter. However, the first superficial constrictor
of elasmobranchs is an obvious serial homologue of the other superficial constrictors
behind it (Fig. 2C), and is unlikely to have evolved independently of those
constrictors. It seems more reasonable to propose that a superficial constrictor gave
rise to the velar muscles than vice versa.
During the evolution of gnathostomes, the main change in the anterior pharynx
was the appearance of jaws. Having argued that the mandibular and hyoid arches
began as typical branchial arches separated by a $1 pouch, I must accept the
classical interpretation of the structural sequence of jaw evolution (see Fig. 16). In
essence, the internal mandibular arch and its musculature enlarged for the bite-like
action of closing off the oral cavity from the pharynx behind it (Fig. 16A, B). As the
jaws enlarged further, the palatoquadrate became horizontal (Fig. 16C).Later, in the
immediate ancestors of sharks, the gape enlarged and the jaws pushed back to brace
against the hyoid arch (Fig. 16D). Behind the jaw joint, at the point of contact
between these two arches, the first gill septum and first constrictor muscle were lost.
At some stage in this sequence, probably after placoderms diverged from other
E.ANCESTOR
F.SHARK
dentides in oral
hyokkan hemibranch
Figure 16. Proposed anatomical stages in the evolution of jaws. Parts A-D show the transition in lateral
view. The internal mandibular arch enlarged, along with the mouth-closing adductor mandibulae
muscle. The hypothetical early gnathostome in Part C has an aphetohyoid or autodiastylic condition, in
which the first gill opening is complete and the hyoid arch is unmodified (de Beer, 1937: 422-425; Stahl,
1974 95; Schaeffer & Williams, 1977). Next, as shown in D, the jaws moved back to brace against the
hyoid arch, squeezing the first gill opening into a dorsal spiracle, in accordance with the aphetohyoid
theory. E and F show the transition in frontal section. In E, a small arrow runs leftward from the adductor
mandibulae, showing how this muscle may have migrated onto the lateral surface of the jaw.
360
J. MALLATT
gnathostomes, teeth evolved from oral denticles (Neal & Rand, 1936; Zangerl, 1981:
6, 36; Reif, 1982: 336; Young, 1986). Tooth derivation is shown in Figure 16E
and F.
The evolution of the jaw-closing adductor mandibulae raises several questions.
This muscle is believed to have had a simple fan shape in early gnathostomes (Fig.
16C)(Allis, 1923; Lauder, 1980a).Although some authors have interpreted it as part
of the interbranchial or superficial constrictor series (Luther, 1938: 504; Lightoller,
1939; Wischnitzer, 1972: 36; Schaeffer, 1975),here it is interpreted as the adductor
branchialis of the mandibular arch (Hughes & Ballintijn, 1965; Romer, 1970: 277;
Wahlert, 1970;Jollie, 1982b). Like an adductor branchialis, it attaches only to the
epi- and ceratobranchial segments (upper and lower jaws), and it adducts these
segments. Furthermore, it does not lie on the gill septum above the palatoquadrate
as do the true first interbranchial and constrictor muscles (i.e. the levator maxillae
and the first dorsal superficial constrictor: Daniel, 1928). The adductor mandibulae
is unusual, however, in lying lateral to its arch (the other adductor branchialis muscles
lie anteromedial to their arches). Evidentally, it originally lay medially but then
migrated laterally as it enlarged, to avoid blocking the oral cavity and to avoid blows
from struggling prey in the mouth. Schaeffer (1975) proposed that placodenns
represent a stage before the adductor mandibulae migrated laterally, but this is
debated (Young, 1986: 22-31).
Outgroup comparison
Other vertebrates. In chimaeroids, the jaw region is more specialized than in sharks
(Dean, 1906: 154):The palatoquadrate is fused into the braincase, and the teeth are
crushing and slicing plates (Patterson, 1992). Furthermore, the largest part of the
ancestral adductor mandibulae, levator mandibulae anterior, has moved far up onto
the skull anterior to the eye, presumably to achieve better leverage for the strong bite
(Edgeworth, 1935; also see Fig. 25). In chimaeroids, the spiracular pouch disappears
during development (Maisey, 1984). Although the functional reason for this loss is
unclear, most other fish with opercula (placodenns, acanthodians, and most
osteichthyans) also lack a spiracular pouch and/or spiracle.
Turning to agnathans, adult lampreys have a velum, but it is smaller than that of
ammocoetes, and it does not pump water. Instead, this hand-shaped structure acts
during feeding to close the entrance to the respiratory pharynx and to open the
esophagus (Kawasaki& Rovainen, 1988). In hagfish, the velum is a posteriorlydisplaced horizontal pump, with two scroll-like strips that propel ventilatory water
into the posterior pharynx (Johansen& Strahan, 1963). It is larger and more complex
than the velum of ammocoetes, but its muscles have the same innervation (V3),and
it is generally considered homologous to the latter (Hardisty, 1979: 73).
Turning to ostracoderms, it already has been argued that osteostracans and
heterostracans had no pumping velum. This raises the problem of how these fish
could have ventilated, because much of their pharynx was enclosed in immobile,
bony shields (Stensio, 1968). The seriousness of this ‘problem’ may have been
overestimated: In osteostracans, water could have been pumped by up-and-down
movements of the flexible pharyngeal floor (Watson, 1954), and in early
heterostracans the sides of the pharynx were covered with branchial scales that
allowed mobility (Elliott, 1987; Wilson & Soehn, 1990). Only in later heterostracans
was the pharynx immobilized in a fully rigid carapace (Denison, 1961; 1964). The
ORIGIN OF JAWS
36 I
pharyngeal walls of hagfih are similarly immobile during ventilation, and because
hagfish rely primarily on a pumping velum, the heterostracans in question are usually
said to have had one too (Stensio, 1968; Moy-Thomas & Miles, 1971). However, it
is not widely appreciated that ventilation in hagfish involves many sets of muscles
besides the velum: muscles around the anterior and posterior parts of the pharyngeal
lumen, muscles around the gill pouches and efferent gill ducts, and interbranchial
muscles called the branchial and cardiac constrictor (Johansen & Hol, 1960;
Johansen & Strahan, 1963: 364-366). If heterostracans lacked a pumping velum as
I propose, their ventilation could have relied on such alternate muscles. Indeed,
heterostracans apparently had muscular gill pouches (Fig. 13A)and efferent gdl ducts
(Denison, 1964: 346). They probably had interbranchial muscles and muscles
near the pharyngeal lumen as well, because these are primitive vertebrate features
(Fig. 4).
Amphioxus and the earliest vertebrates. Continuing with the outgroup comparisons, the
anterior pharynx of amphioxus will be considered next (Fig. 17). Amphioxus
probably resembles pre-vertebrates in many ways (Garcia-Fernandez & Holland,
1994),so it should provide clues to the organization of the vertebrate head that are
relevant to the present study. As in ammocoete lampreys, a velum marks the
entrance to the pharynx, posterior to which lies a ciliated peripharyngeal groove,
then the first branchial slits and bars (cf. Fig. 17 and Fig. 2B). The ring-like velum of
amphioxus develops where ectoderm meets endoderm in the region of the
mandibular somite, as does the velum of embryonic lampreys, so the two are in
corresponding positions (Jefferies, 1986). The inner edges of the amphioxus velum
bear sensory tentacles that monitor the chemistry of inspiratory water (Bone, 196l),
in a way analogous to the presumed water-sensing function of a fish pseudobranch.
vdum (with sphincter)
ub-shaped gland (in larva)
oral hood and oral cavity
Figure 17. The cephalochordate, amphioxus. This mid-sagittal cut through the mouth and pharynx is
modified from figures 3.3 and 3.5 in Jefferies (1986). As in lampreys, a velum defines the anterior
boundary of the pharynx. Here, however, the velum is not a ventilatory pump. The club-shaped gland
is present only in the larval stage, and is included in this adult picture for illustrative purposes only.
362
J. MALLATT
Behind this, the complex pattern of intrapharyngeal ciliated bands is nearly identical
to that in the ammocoete pharynx, so it is likely that the peripharyngeal groove of
amphioxus is homologous to the pseudobranchial groove of ammocoetes (Mallatt,
1984b). Thus, the peripharyngeal groove marks the ‘hyoid’ region in amphioxus. A
spiracular pharyngeal pouch is expected between the velum and the peripharyngeal
groove, and this may be represented by a club-shaped gland in larval amphioxus
(Goodrich, 1930b). Like a spiracular pouch, this gland is a tube extending from the
exterior to the pharyngeal lumen. Intriguingly, Olsson (1983)found that water from
the exterior flows inward through the club-shaped gland to enter the pharynx, the
same direction in which water travels through a fish spiracle.
Unlike the ammocoete velum, the velum of amphioxus is not a ventilatory pump
(water is moved through the pharynx by the pumping action of cilia on the branchial
bars). Instead, the amphioxus velum acts like the iris of an eye (Ayers, 1931) to
control the amount of water entering the pharynx (Jorgensen, 1966: 127). In closing
and opening the entrance to the pharynx, it functions like the oral valve of
Chondrichthyes and the medial velar flaps of ammocoetes.
What can the anterior pharynx of amphioxus reveal about the earliest stages in
vertebrate evolution, the chordate-to-vertebrate transition? In fish, the structures in
this part of the pharynx are markedly gill-like. Illustrating this, the mandibular region
of sharks has its own gill ‘filaments’ (pseudobranch), internal branchial arch (jaws),
gdl septum, and interbranchial and branchial constrictor muscles. By contrast, the
homologous structures in amphioxus - the velum and anteriormost pharyngeal
wall - bear little resemblance to the branchial bars and gill slits behind them. For
instance, the velum of amphioxus contains no branchial bar. Gans (1989, 1993)
considered the chordate-to-vertebratetransition to be a period when an amphioxuslike ancestor developed true gills, and evolved cartilaginous branchial arches along
with ventilatory muscles. Assuming this is true, then these ventilatory changes swept
so far forward in the evolving vertebrate pharynx that they also ‘branchialized’ the
previously dissimilar velar region.
If the anterior pharynx of pre-vertebrates was not gdl-like, then certainly these
ancestors had no ?re-mandibular’ gill structures in front of the pharynx. Although
many earlier workers believed that such premandibular gdls and arches once existed
in the oral cavity (see reviews in Sewertzoff, 1928, and Jollie, 1968), most modern
authors reject that idea (Moy-Thomas & Miles, 1971; Schaeffer, 1975;Jollie, 1977;
1982a; Hardisty, 1981: 358;Jefferies, 1986: 119; Maisey, 1989). The main evidence
against premandibular branchial structures is that the oral cavity of vertebrates
develops from an embryonic chamber (stomodeum)that is clearly separated from the
pharynx behind it by the buccopharyngeal membrane, and the stomodeum has
never convincingly been shown to contain lateral pouches comparable to gdl
pouches (Goodrich, 1930c: 48; Claydon, 1938: 12). Nor does the oral cavity of
amphioxus offer any evidence for premandibular gdl elements (Fig. 17). This region
does not even exist until the amphioxus metamorphoses, then it appears as the
unpouched space between the right and left walls of an oral hood (Ayers, 1931;
Jefferies, 1986; Stokes & Holland, 1995).
The conclusion that no vertebrate ever had gill structures anterior to the
mandibular arch has several implications, which have not been explored fully in the
literature. First, it negates the classical interpretation of the maxillary nerve (V2),
which supplies the snout and dorsal mouth anterior to the pharynx, as part of a
premandibular branchial nerve (Goodrich, 1930a; Smith, 1959; Stensio, 1968).That
ORIGIN OF JAWS
363
is, V, cannot be a pretrematic branch associated with some lost premandibular pll
slit. This is impossible for two other reasons as well. First, agnathans lack pretrematic
branchial nerves (Whiting, 1977), yet lampreys do have a V2, which innervates
exactly the same head regions as in gnathostomes (Northcutt & Bemis, 1993).
Second, true pretrematic branchial nerves are strictly sensory in function, yet V2 in
lampreys and chimaeroids contains both sensory and motor axons - as do the
branches of the trigeminal supplying the snout of hagfish (Holmgren, 1942: 249;
Lindstrom, 1949; Peters, 1963).It seems that V, primitively was a mixed nerve to the
head, rather than a pretrematic branchial nerve.
Furthermore, if premandibular branchial arches never existed in vertebrates, they
cannot have given rise to the trabeculae of the embryonic skull. Previous authors
proposed such a derivation because the trabeculae, like branchial arches, develop
from neural crest (de Beer, 1937; Schaeffer, 1975). More recently, however, it was
demonstrated that neural crest inherently forms the parts of the skull rostral to the
notochord, independent of its contribution to the branchial arches (Langille & Hall,
1988; Couly et al., 1993).
Section 3: Lips and mouth
As in other sections of this paper, the oro-labial region of ammocoetes and
Chondrichthyes will be described as a basis for reconstructing this region in the
common ancestor. However, these structures will be considered in more detail
because they are not well described in the literature. Chimaeroid fishes are especially
important here, and will be described along with ammocoetes and sharks. Among
chimaeroids, the focus will be on the genera Chimaera and Hydrolagus rather than
Callorhinchus, because the lips of the latter seem modified for feeding on infauna
(Ribbink, 1971: 69).
Comtructirg the ancestral lips and mouth
Sufme appearance in extant animal. In ammocoetes (Fig. 18), the latmal and lower lips
form a semicircular ridge around the ventral two-thirds of the round mouth opening.
The dome-like upper lip is large, mainly consisting of right and left vertical walls.
Burrowing ammocoetes use this muscular structure to feel whether sediment is soft
enough to enter, and then as a pointed probe to push through this sediment (personal
observation, and Hardisty & Rovainen, 1982: 140). Altogether, the upper lip and
mouth region resemble a pitcher plant, and trap algae and detritus rolling along the
stream bed in the same way the plant traps insects. Some tentacles (cirri, papillae) hang
from the ceiling of the upper lip, while others surround the mouth opening just
posterior to the lips. These tentacles keep large particles from entering the mouth of
microphagous ammocoetes (Youson, 1981; Sanderson & Wassersug, 1993). Behind
the tentacles and lips lies the oral cavity and velum (Fig. 2B). The oral cavity has
cheek-like lateral walls (Fig. 18B), and its floor has a ventral longitudinal crest, which
supports an especially large tentacle (Fig. 18A). The unpaired nostril of lampreys has
an unusual, dorsal location (Fig. 18B). In embryos, it fist forms in a terminal
position, then is shifted dorsally by the tremendous growth of the upper lip (Schaeffer
& Thomson, 1980; Gorbman & Tamarin, 1985). The unpaired nature of the nasal
J. MALL4TT
364
A
Figure 18. Lips and mouth of an ammocoete. A, anterior view; B, lateral view. Drawn from preserved
specimens of Pefrmnyzonmminus (A) and Lumflfru plnnm' (B).
apparatus seems to be a derived character, because embryonic lampreys start with
paired olfactory pits (Neal & Rand, 1936: 574; Johnels, 1948: 164).
The following description of the mouth and lips of Chondrichthyes is based largely
on preserved specimens of Squalus ucunthias and Chimaera monstrosa, and much of it
apparently is new to the literature (but see Allis, 1919, and Compagno, 1989: 19).
Sharks will be considered first (Fig. 19).The mouth opening is not round, but slit-like,
with lateral corners that reach posterior to the eye region. Although t h i s opening is
relatively small in Squalus, primitive sharks and bony fish had longer jaws and large
mouth openings (Moy-Thomas & Miles, 1971). The lateral lip is a distinct ridge
called a tabidfold (Walker, 1965: 32):Ventrally, this fold continues for only a small
distance onto the lower jaw then fuses to the latter. Thus, there is no lower lip.
(However, I observed that the lower lip is complete in long-jawed shark Heptrunchias
pe~lo,separated from the mandible by a cleft). The upper lip of Squulus has two parts:
a thin, medialjup of skin that is separated by a slit from the palatoquadrate; and
wedge-shaped lateralfoldc of& upper lip. I consider these lateral folds (plus a short
region medial to them: see below) to be homologous to the upper lip of ammocoetes.
When the lateral fold and labial fold are pulled forward (Fig. 19B), they are seen to
be continuous with a mucosal buccal numbrune, which lies in a deep labialpouch (Fig.
19A and Wischnitzer, 1972: 25). The buccal membrane lies anterior to the jaws, and
it occupies the same position as the lateral wall of the oral cavity of ammocoetes.
Therefore, I consider these two cheek structures to be homologous. When a shark
opens its mouth to suck in prey, the lateral fold, labial fold, and buccal membrane
project forward. This rounds the mouth opening, assuring that effort is not wasted
sucking water into the corners of a grin-shaped mouth (Alexander, 1978: 95).
The shark Squalus has a homologue to the oral cavity of ammocoetes. This
premandibular region is the space internal to the labial folds and buccal membrane,
as well as the slit between the medial flap of the upper lip and the palatoquadrate
cartilage.
The paired nostrils of Squulus lie far anterior to the mouth, on the undersurface of
the long rostrum. In primitive sharks, however, a rostrum was lacking and the nostrils
ORIGIN OF JAWS
365
rostrum
A
labial fold
-
labial fold
B
buccal munbme
labiaifold
Figure 19. Lips and mouth of a shark, Sqwh acmthias. A, ventral view; B, lateral view. In the small
picture below A, the lateral fold of the upper lip is lifted to show the underlying structures. In B,this fold
is pulled forward to reveal the structures in the labial pouch (stippled).Notice the levator labii superioris
muscle in the cheek-lie bucchal membrane. Drawn from a preserved specimen.
366
J. MALLA'IT
occupied a terminal position just above the mouth, as in modern hexanchiform
sharks like Chlamydosehhus (Zangerl & Williams, 1975; Compagno, 1977: 305).
Oro-labial structures were examined in other shark species. Those of Squatina
calijimica and Trialcis semijimciutus are basically the same as in Squalus acanthb.
Together, these three animals represent the three Werent superorders of extant
sharks (accordingto the phylogeny of Compagno, 1977),suggesting that their similar
oro-labial structures are plesiomorphic. The similarities also hold for Gingylostoma
cirratum and Hehodontus japonica, although in these sharks a slit from each nostril
separates the lateral fold from the rest of the upper lip. In highly pelagic predators
such as Chhydosehhus anguineus, Heptranchius perlo, Carcharinus sp., and Sptyrna lmini,
the oro-labial structures are small, and the lateral fold of the upper lip may be absent.
This reduction may relate to the fact that some of these sharks feed by biting and
gouging pieces from large prey, rather than by sucking prey into their mouths (Moss,
1977).
Turning to chimaeroids, the lips and mouth of Chimaera monstrosa resemble those
of ammocoetes in some ways and those of sharks in others (Fig. 20). As in
ammocoetes, the mouth opening is relatively small. It has lateral corners but these do
not reach as far posteriorly as the eye region. The lower lip is a well-developed ridge.
The lateral lip is a broad lubialfoZd, as in Squalus. The upper lip consists of a medial
part (hke the medial flap in sharks, but thicker and pad-like) and two lateral vertical
flaps called nasolabialfolrls (Allis, 1917). The latter are separated by the nostrils but
otherwise resemble the upper lip of ammocoetes. The labial pouch is developed to
different degrees in different specimens, but is always shallower than in Squalus (Fig.
20C). The deepest parts of this pouch may be lined by mucosa but in general the
cheek-like lateral walls of the oral cavity are covered by skin (as in ammocoetes).
Internally, the premandibular oral cavity is larger than in sharks because the lateral
and lower lips extend farther forward from the jaws. The paired, terminal nostrils of
chimaeroids lie just above the mouth opening, which matches the proposed positions
of the nostrils in the ancestors of both sharks and lampreys (see above).
The oro-labial structures of other chimaeroids were examined (Hydrolagus colliei,
Callorhinchus milii, and Rhinochimaera paqfica), and found to have all the features
described for Chimaera monstrosa. However, the lips of Rhinochimaera p 4 c a are
especially large and robust, and each nasolabial fold is crinkled into anterior and
posterior parts in Callorhinchus (also see Kesteven, 1933).
The lips of chimaeroids seem to function like those of sharks. Hydrolagus colliei were
observed feeding on shrimp at the Seattle Aquarium, and the lips were manipulated
in a freshly dead specimen. Results suggested that the act of opening the mouth to
suck in prey automatically projects the cheek forward and causes the nasolabial and
labial folds to round the mouth opening.
Oro-labial shkton in extant animals. In ammocoetes (Fig. 21A), the skeleton of the lips
and mouth consists of the rostro-dorsal plate, lateral mouth plates, and ventro-lateral
plate, all composed of mucocartilage (Johnels, 1944, 1948).The subcutaneous, rostrod o r s u l p b is the skeleton in the upper lip. Posteriorly, it attaches to the nasal capsule
and to the anterior wall of the fibrous braincase just behind the nasal capsule
(personal observations on sectioned Petromyzon marinus). O n each side, a subocular
process extends back inferior to the eye. The paired lateral mouth plates are bars that
form a ring around the mouth opening, just posterior to the lateral and lower lips
(Figs 21A, 22A). They lie deep in the lateral wall of the oral cavity, separated from
ORIGIN OFJAWS
367
L
h
G
\
/
amd
B. SHARK
d
v
e tissue to
ethnuGdbreincase
A AMMWOETE
vcntro-iateral plate
c. CHIMAERA
Figure 22. Schematic diagrams of the mouth regions of an ammocoete (A), shark (B), and Chimncra (C), showing the relationships of the skeletal elements to other oral
structures. These views look straight into the mouth opening. In all three animals, upper-lip cartilages (marked with crosses) lie anterior to oral cartilages (markedby stippling)
that occupy the lateral walls of the oral cavity and join dorsally to the ethmoid braincase. Internal to the oral cartilages lies the oral mucosa. Part B is based on Squzlur
acanthins.
W
m
W
370
J. MALLATT
that cavity by a small artery. Despite this deep location, each lateral mouth plate
sends a lateral process superficially into the posterior part of the upper lip. Dorsally,
just behind the nasal capsule, the lateral mouth plates fuse to the trabecular
cornmissure and fibrous walls of the braincase (Fig. 22A). Here, they lie deep to the
subocular processes of the rostro-dorsal plate. Functionally, the lateral mouth plates
seem to hold the mouth open, and they must recoil to re-open the closed mouth upon
relaxation of the oral sphincter muscle (elevator labialis ventralis: see below).
Additionally, they support the oral tentacles (Gaskell, 1908;Johnels, 1944: 72), for
they are continuous with the mucocartilaginous cores of such tentacles (Fig. 15B).
The ventro-lateralplate is a thin, subcutaneous sheet in the floor of the oral cavity and
anterior pharynx. It lies external to the lateral mouth plates, velar skeleton, and all
muscles.
The lateral mouth plates of ammocoetes bear a superficial resemblance to the
branchial arches behind them, and repeatedly have been called a premandibular
branchial arch (for reviews, see Claydon, 1938;Johnels, 1948; and Hardisty, 1981).
I already argued that this is incorrect, that branchial arches cannot exist in the
mouth. As hrther proof of this, the lateral mouth plates do not fit the criteria of
either an external or internal branchial arch: They lie too far medially to be an
external arch, but unlike internal arches they lie external to their arteries (Fig.
22A).
In sharks, the skeleton of the lips and mouth is formed by labial cartihgtx These are
rather uniform among the different groups of extant sharks (Holmgren, 1942: 246)
and consist of anterior, posterior upper, and posterior lower, pairs (Figs 21B, 22B).
A flat, triangular anterior labial cartilage occupies the lateral fold of each upper lip,
although one-third of the cartilage lies medial to this fold in Sqwlus. In location, this
cartilage is comparable to the rostro-dorsal plate in the upper lip of ammocoetes.
Although it differs from the rostro-dorsal plate in lying posterior instead of anterior
to the nasal capsule, a ligament attaches it to the braincase just behind the nasal
capsule in most sharks (Allis, 1917: 125-126; 1923: 164). This attachment is exactly
where the rostro-dorsal plate joins the braincase in ammocoetes (cf. Fig 21A and
2 1B). Deep to the anterior labial cartilage, the posterior upper and posterior lower labial
cartilages form a ring around the mouth opening of sharks, as do the lateral mouth
plates of ammocoetes (Fig. 22B). During suction feeding in sharks, these cartilages
support the forwardly projected cheek (Wu, 1994). Dissections of Squulzls acanlhiar
reveal that the posterior labial cartilages lie in the buccal membrane posterior to the
labial fold (Fig. 19B), in the same position as the lateral mouth plates (Fig. 21); and
they likewise join dorsomedially to the post-nasal ethmoid braincase, through a thin
layer of connective tissue (see Fig. 22B). They lie medial to the anterior labials (AUis,
1923),just as the lateral mouth plates lie medial to the posterior parts of the rostrodorsal plate in ammocoetes (Fig. 21). Although they often have been called
premandibular branchial arches (Goodrich, 1930a: 448), the anterior and posterior
labial cartilages are better interpreted as homologues of the rostro-dorsal and lateral
mouth plates of ammocoetes.
Labial cartilages were dissected in some other shark species. In Sqwtina calijirnica,
they occupy the same locations as in Sqwlus, but the posterior labials are larger and
they raise ridges on the body surface just posterior to the lips. No labial cartilages
were found in the hammerhead Sphym Mi,
whose lips are extremely reduced. In
Carcharhinus sp. and T f i semfmktus, the anterior labial cartilage extends from the
lateral fold of the upper lip to a position far anteromedial to this fold, under the flat
ORIGIN OF JAWS
371
skin on the palatoquadrate. I consider the entire region occupied by this cartilage in
sharks to be homologous to the upper lip of ammocoetes.
In my dissections of Squalus and Heptranchiusperlo, a subcutaneous sheet of fibrous
tissue was discovered on the undersurface of Meckel’s cartilage and the posterior
lower labial cartilage (see Figs 21B and 22B). Thisfibrous sheet has the same relative
location as the ventro-lateral plate of ammocoetes.
In Chimaera, the skeletal elements of the lips and mouth region are the prelabial
and maxillary labial cartilages (terms from Holmgren, 1942), and a fibrous mass in
the lower lip (Figs 2 lC, 22C). The triangular prelabial cartilages feel soft to the touch.
They are in the nasolabial folds, the same ‘upper-lip’ location as the rostro-dorsal
plate of ammocoetes and anterior labial cartilages of sharks (Fig. 2 1). Each prelabial
cartilage articulates posteriorly with a trapezoidal maxillaty labial cartiluge, the main
part of which lies in the cheek just behind the mouth opening. However, a lateral
process projects superficially from this labial cartilage into the posterior part of the
nasolabial fold (upper lip). Based on its location and its lateral process, the maxillary
labial cartilage seems homologous to the lateral mouth plate of ammocoetes and,
therefore, to the posterior labial cartilages of sharks. The prelabial and maxillary
labial cartilages of Chimaera meet directly posteroinferior to the nasal capsule, as do
the two corresponding cartilages in ammocoetes.
This interpretation raises several potential problems, which should be addressed.
First, the single prelabial cartilage of Chimaera corresponds to a series of three upperlip cartilages in Rhinochimaera and Callorhinchus (premaxillary, pedicle, and prelabial
cartilages: Holmgren, 1942), and this multi-cartilage condition is probably primitive
for chimaeroids (D.A. Didier, personal communication). This does not invalidate the
homologies that are claimed here, however, because the rostro-dorsal plate of older
ammocoetes also consists of several distinct pieces (Johnels, 1944: 72). The mmillaty
labial cartilage is also divided in Rhinochimaera and Callorhinchus, into superior and
inferior pieces. This subdivision may be a specialization to allow easier bending when
the mouth closes, for a similar specializationoccurs in some orectoloboid sharks (Wu,
1994).
The triangular fibrous muss in the lower lip (Jollie, 1962: 123) underlies Meckel’s
cartilage in chimaeroids. It was, indeed, entirely fibrous in my specimens of Chimaera
monstrosa (Fig. 2 1C). However, it is cartilaginous in Rhinochimaera and Callorhinchus (the
premandibular cartilage: Holmgren, 1942). Lying superficial to all muscles, this
fibrous mass has the same location as the ventro-lateral plate of ammocoetes and the
submandibular fibrous sheet in sharks.
Oro-labial muscles in extant animals. In ammocoetes, the oro-labial musculature is
complex, and the sectioned Petromyzon marinus of the present study differed in some
ways from the descriptions in the literature (Tretjakoff, 1929; Damas, 1935; Hardisty
& Rovainen, 1982).In the upper lip, the largest and most important muscle is bucca6
anterior (Fig. 23A). My sections reveal that its origin is extensive, from the
superolateral walls of the oral cavity, the superoanterior surface of the lateral mouth
plate, the trabecular commissure just below the nasal capsule, and the nasal capsule
itself. It forms most of the mass of the upper lip and inserts onto the entire
undersurface of the rostro-dorsal plate and onto the lip mucosa. Functionally,
buccalis anterior retracts and constricts the upper lip (Hardisty & Rovainen,
1982).
Other muscles surround the oral cavity and mouth opening of ammocoetes (Fig.
372
A
B
C
deMtor labidis ventralis
F w r e 23. Muscles and nerves of the lips and mouth of ammocoetes. A, attachments of buccalis anterior,
the main muscle of the upper lip; B, rnusdes around the oral cavity and mouth opening, and the paths
of the maxillary (VJ and mandibular (V,) nerves; C, ventral view, showing how the elevator labdis
ventralis and buccal constrictor overlap on the floor of the oral cavity. A and B are based on serial sections
through Petrmnyzon mWinur, and C was dram &om a preserved specimen of Lmnpcha fiW.
ORIGIN OF JAWS
373
23B): buccal constrictor, elevator labialis ventralis, sublabialis, and basalis tentacularis. Judging from my serial sections, the buccal constrictor encircles the oral cavity
from the external hyoid bar posteriorly to the front of the eye anteriorly. It forms the
bulk of the ‘cheek’. Superiorly, it attaches to the trabeculae and the fibrous braincase.
Ehator labialis ventralis surrounds the mouth opening. It seems to be an anterior
continuation of the buccal constrictor, because it grades into the latter ventrally (Fig.
23C). As it ascends, this elevator muscle lies directly anterior to, then directly lateral
to, the lateral mouth plate (Fig. 23B). Superiorly, it runs along the undersurface of
the posterior part and subocular process of the rostro-dorsal plate, then attaches to
the fibrous braincase between the eye and nasal capsule. Besides raising the lower lip,
it must act as an oral sphincter. In my sections, the sublabialis muscle differed from
literature descriptions. Both Tretjakoff (1929) and Damas (1935) said this muscle
originates along a bar of mucocartilage in the ventral longitudinal crest and ascends
into the oral tentacles (for this reason, Damas re-named it ‘‘m. retractor papillaris”).
In the present study, the origin was confirmed, but the muscle ascended anterior to
the lateral mouth plate and inserted on the rostro-dorsal plate lateral to the nasal
capsule. It did not send slips to the tentacles. This suggests that the sublabialis does
not retract the tentacles, but helps close the mouth by pulling down on the upper lip
and pulling up on the floor of the oral cavity. The true retractor of the tentacles was
discovered as a distinct, thin-fibered muscle in the anterior part of the oral cavity,
along the bases of the tentacles. This new muscle was named basalis tentacuh?7j (Fig.
23B).
Although the present study has re-defined a few oral muscles of ammocoetes, the
general pattern of their innervation remains clear. The maxillary (V2:suboptical) and
mandibular (V,) nerves both run through the oro-labial region (Fig. 23B). Mostly, V2
innervates the dorsal muscles, V3 the ventral ones (Gaskell, 1908: 289). More
specifically, V, innervates the muscles of the upper lip including buccalis anterior,
and V3 innervates the circumoral muscles, i.e. buccal constrictor and sublabialis
(Hardisty & Rovainen, 1982). As for the elevator labialis ventralis, Tretjakoff (1929)
claimed it was innervated superiorly by V2 (ramus apicalis). However, he may have
confused the superior part of this muscle with some other, because he wrongly
claimed it inserted on the upper lip. On the other hand, Lindstrom (1949: 371)
traced V3 into the ventral part of the elevator labialis ventralis (which he called the
part of the buccal constrictor lying rostral to the lateral mouth plate). Alcock
recorded the same thing (see figure 1 14 and page 289 in Gaskell, 1908). Therefore,
it seems likely that elevator labialis ventralis is innervated by V3 rather than V2.
In sharks, the oral musculature is simpler than in ammocoetes (Fig. 24). Whereas
the upper lips of ammocoetes are highly muscular, those of sharks lack muscle. That
is, no muscles attach to the anterior labial cartilages (Allis, 1923; and personal
observation).Correspondingly, V2 has no motor axons and is strictly a sensory nerve
in sharks and in the teleostome gnathostomes.
(also
The only muscle around the mouth opening of sharks is levator hbii suflm’o~
called preorbitalis and suborbitalis).This muscle originates on the ethmoid region of
the braincase between the two eyes just rostral to the palatoquadrate (Figs. 22B, 24).
In Squalus, it runs back behind the posterior labial cartilages and inserts by a thin
tendon onto the adductor mandibulae muscle. In other sharks, however, it extends
farther ventrally to insert on Meckel’s cartilage (Daniel, 1928: 95; Lightoller, 1939:
360; Edgeworth, 1935: 46; Wu, 1994). Functionally, this muscle protrudes the lips,
buccal membrane, and labial cartilages to round the mouth opening during suction
J. W l T
374
feeding (Moss, 1977). It may also help close the mouth (Edgeworth, 1935: 46;
Gilbert, 1973), and in some advanced sharks it protrudes the palatoquadrate
(Frazetta and Prange, 1987; Wu, 1994). It is innervated by V3. In its location,
attachments, innervation, and presumed mouth-closing function, the levator labii
superioris of sharks resembles the buccal constrictor of ammocoetes, so these two
muscles should be homologous.
This claim for homology might be questioned on the grounds that levator labii
superioris is widely considered to be part of the adductor mandibulae (Edgeworth,
1935; Romer, 1970; Lauder, 1980a).My counterargument is that it is separate from
A
B
Figure 24. Muscles and nerves of the 'cheek' and mouth of sharks. A, levator labi superioris and adductor
mandibulae muscles in Squalus acrmthias (drawn from a preserved specimen); B, levator labi superioris in
Chlmnydosdzchus rmguineus, and its relations to the nearby nerves and labial cartilages (after Mi, 1923).
ORIGIN OF JAWS
375
the adductor mandibulae in sharks and bony fish, and it does not originate on the
palatoquadrate in sharks, as should a part of the adductor mandibulae. Levator labii
superioris is said to develop from the embryonic adductor mandibulae (see page 45
and figure 107 in Edgeworth, 1935), but this is a matter of interpretation: Viewing
Edgeworth’s figure, I interpret it as developing from the anterior part of the
mandibular branchiomere, the rest of which becomes adductor mandibulae. (The
buccal constrictor of lampreys also develops from this branchiomere: Hardisty &
Rovainen, 1982: 139).In open-mouthed sharks, levator labii superioris is seen in the
buccal membrane anterior to the jaws, not in the adductor mandibulae (Fig. 19B).
Viewed this way, it is a premandibular cheek muscle like the buccal constrictor of
ammocoetes.
In Chimaera (Fig. 25) the lip and mouth muscles seem comparable to those of
ammocoetes. Three muscles attach to the prelabial cartilage in the nasolabial fold,
and can be called upper-lip muscles: levator anguli o k anterior, labialis anterior, and levator
prelabialis (Edgeworth, 1935; Holmgren, 1942).They run from the pre-orbital part of
the braincase and the maxillary labial cartilage to the prelabial cartilage, much as the
buccalis anterior of ammocoetes runs from the anterior braincase and lateral mouth
plate to the rostro-dorsal cartilage in the upper lip. The claim that the three upper-lip
muscles of chimaeroids are homologous to the buccalis anterior of ammocoetes is
levator
anguli oria
anterior
cephalic
clasps
\
levator
anguli oris
posterior
otic process of
palatoquadrate
I
I
I
/ I
anterior
oosterior
I
fibrous mass
in lower lip
PharYngOhYd
I
I
?
/
/ I
--
\-
\
hyoid arch
EarY
Cartilage
Figure 25. Oro-labial muscles and nerves in Chimnera monrhosa. The V,-innervated muscles to the upper
lip are levator anguli oris anterior, labialis anterior, and levator prelabialis (the latter is rudimentary in
Chimaera but large in other chimaeroid genera such as Cuffmhinchur:Edgeworth, 1935). The inset at upper
right shows the hyoid arch, including its pharyngohyal segment. Drawn from a preserved specimen.
316
J. MALLAlT
strengthened by the fact that both sets of muscles are innervated by V2 - and the
chimaeroid muscles are the only V2-innervated muscles known in gnathostomes (see
Holmgren, 1942). Indeed, there is reason to believe this is a shared primitive
condition retained by lampreys and chimaeroids, because V2 muscles, once lost in
sharks and teleostomes, never re-evolved. (”he analogous muscles in the lips and face
of mammals evolved from neck muscles and have a different innervation, the facial
nerve.)
Once the chimaera Hydro@ collia’ sucks food from the sediment surface, it
initiates a series of chewing movements, rapidly protruding then retracting the cheek
and lips (personal observation). The V2-innervated muscles may help to perform
these functions.
Turning from the labial to the oral muscles of chimaeroids, the thin labialis posterior
curves like a sling around the floor of the mouth just posterior to the lips. (A similar
muscle called labialis inf.im is said to lie posterior to this,but was not found in the
present dissections: Edgeworth, 1935; Stahl, 1967: 180). The labialis posterior
extends from the superior anterior margin of the maxillary labial cartilage down
across the ventral surface of Meckel’s cartilage and deep to the fibrous mass in the
lower lip (Figs 25,22C). Functionally, this muscle could weakly lift the lower lip and
mandible. It is innervated by Vs. In position and innervation, it resembles the
similarly sling-like elevator labialis ventralis of ammocoetes. Finally, a large muscle
just posterior to labialis posterior, levutor unguli oris posterior (V3),could be homologous
to the buccal constrictor of ammocoetes and the levator labii superioris of sharks.
Like those muscles, it originates from the suborbital braincase, lies directly posterior
to the maxillary labial cartilage ( = lateral mouth plate; = posterior labial cartilages),
and occupies the cheek anterior to the mandibular arch and jaw joint (Fig. 25).
To summarize the above, basic similarities exist between the muscles of
chimaeroids and ammocoetes: In both animals, V2-innervatedmuscles run from the
anterior part of the braincase to the upper-lip cartilage, while V3-innervated muscles
encircle the mouth opening and the cheek behind the lateral and lower lips. These
proposed muscle homologies could be tested definitively by mapping the cell bodies
of V2- and V3-motor neurons in the brain stem of chimaeroids, then comparing the
map with the ammocoete map obtained by Homma (1978).
Evuluating the homologies. Table 1 summarizes all the proposed homologies in the
mouths and lips of ammocoetes, sharks, and chimaeroids. These are very different
types of animals (jawlessversus jawed fish), so it is necessary to consider whether the
proposed homologies are reasonable. The fossil record poses no problem, because it
indicates that labial cartilages existed in early placoderms, chimaeroids, sharks, and
perhaps even in acanthodians (Patterson, 1965; Moy-Thomas & Miles, 1971: 179;
Maisey, 1983; Long, 1986). Still, the homologies should be evaluated more
thoroughly. One way to do this is by checking whether the oral cartilages and
muscles of the various animals relate similarly to nearby arteries and nerves.
The arteries will be considered fist. In all three animals, oral arteries pass medial
to the oral cartilages. In ammocoetes, a vertical artery that connects the external
carotid below with the orbital artery above lies medial to each lateral mouth plate
(Con, 1906, cited in Claydon, 1938). Likewise, in Squallls I found a branch of the
external carotid artery ascending medial to the posterior lower labial cartilage (Fig.
22B). Similarly, in Chimaera, the labial cartilages are “lateral... to the branchial
arteries” (Stahl, 1967: 173).
TABLE
1. Proposed homologies in the mouth and lips of ammocoete lampreys, Chondrichthyes, and other chordates
Ammocoetes
1. SURFACE SI'RUCWRES
lower lip
lateral lip
upper lip
lateral wall of oral
(cheek)
oral cavity
mouth opening
velum
medial flap of velum
2. SKF.LETON
rostro-dorsal plate
lateral mouth plate,
with lateral process
ventro-lateral plate
3.MuscLFs
buccalis anterior (Vz)
Sharks (Squulus)
Chimaera
Vertebrate ancestor
-
lower lip
labial fold
nasolabial fold
lower lip
lateral lip
upper lip
lateral wall of oral cavity
(cheek)
slit between lip, cheek,
and jaw
mouth opening
jaws
cheek
labial fold
lateral fold of upper lip
(and region medial to it
that likewise contains the
anterior labial cartilage)
buccal membrane (cheek)
slit between lip, cheek,
and jaw
mouth opening
jaws, pseudobranch, and
first superficial constrictor
buccal constrictor (v,)
mouth opening
mandibular hemibranch,
and first superficial
constrictor
oral valve
Amphioxus
skin over cornual
cartilage, and cornuosubnasal muscle
none
lateral wall of oral
cavity
oral cavity
oral hood
mouth opening
velum
margin of oral hood
velum (but no
superficial constrictor)
?
medial part of velum
oral valve
oral valve
anterior labial cartilage
posterior labial cartilages
prelabial cartilage
upper-lip cartilage
maxillary labial cartilage, oral cartilage
with lateral process
fibrous mass in lower lip fibrous or cartilaginous
sheet
cornual cartilage
labial, or coronary,
cartilage
levator prelabialis, levator upper-lip muscles
anguli oris ant, labialis
anterior (Vz)
labialis posterior (V,)
oral sphincter
cornuosubnasalmuscles
fibrous sheet on Meckel's
cartilage
-
elevator labialis ventralis (V3)
ancestral oral cavity
Hagfish
levator labii superioris (V,)
levator anguli oris
posterior (V,)
buccal constrictor
coronarious
basitentacularis
levator cartilaginis
basalis, protractor
cartilaginis basalis,
cmiobasialis
oral cavity
0
62
B
>
3
4
hoop formed by bases
of tentacular cartilages
pen-buccal muscles
-
-
w
U
378
J. MALLAlT
Turning to the nerves of the lips and mouth, the path of V2 seems comparable in
all three animals. In serial sections of ammocoetes, V2 runs anteriorly through the
oral region lateral to the buccal constrictor, elevator labialis ventralis, and lateral
mouth plate (Fig. 23B). Near that plate, it splits into two branches (Lindstrom, 1949):
(1) ramus apicalis, which turns medially and enters the upper lip deep to the rostrodorsal plate; and (2) ramus suborbitalis, which runs laterally and supplies the skin of
the upper lip superficial to the rostro-dorsal plate. Posterior to the upper lip, V2 lies
lateral to buccalis anterior; but in the upper lip, its ramus apicalis runs medially
through that muscle. The path of V2 in the shark Chlamydoselachus (Allis,1923)
resembles that in ammocoetes: As shown in Figure 24B, V2 runs lateral to levator
labii superioris and the posterior upper labial cartilage, then deep to the anterior
to the latter cartilage to
labial cartilage. Additionally, some of its fibres run mp+Z
reach the overlying skin of the upper lip (these lateral fibres were described by Allis
as belonging to the buccal nerve to the lateral line, but cutaneous fibers of V2 are
always mixed into that buccal nerve: Hyman, 1942: 467). In Squalus, I found the
infraorbital nerve (mixed V2 and buccal nerve) to have similar relationships: Below
the eye, it lies on the lateral surface of levator labialis superioris and the posterior
upper labial cartilage, and sends one end-branch deep to the anterior labial cartilage.
Another end-branch, extending posteriorly from the preorbital process of the skull,
passes superficial to this cartilage. In Chimaera (Fig. 25), as V2 runs toward the upper
lip it lies lateral to the levator anguli oris anterior and labialis anterior muscles (just
as V2 is lateral to the posterior parts of buccalis anterior in ammocoetes); distally, it
splits into two branches, one deep and the other superficial to the prelabial cartilage
in the upper lip (Allis, 1917: 130; and personal observation)-exactly as in
ammocoetes.
The course of the final part of the mandibular nerve (V,) is also comparable in the
three animals (Figs 23B, 24A, 25). In ammocoetes (Lindstrom, 1949: 37 1) and Squalus
(personal observation),V3 descends to the floor of the mouth, turns anteriorly, then
runs through the buccal constrictor (it runs through the tendon of levator labialis
superioris in SquaZus). It continues along the lateral surface of the lateral mouth plate
(ammocoete)or posterior lower labial cartilage (shark)and deep to the ventro-lateral
plate (ammocoete)or fibrous sheet (shark), to end in the skin of the lower lip region.
In Chimaera,the situation is complicated by the fact that levator anguli oris posterior
and the maxillary labial cartilage end rather high, so that V3 passes just inferior to
these structures (Fig. 25); however, V3then runs deep to the fibrous mass to reach the
skin of the lower lip, as in the two other animals.
It is concluded that the paths of V2 and V3 are similar in ammocoetes, sharks, and
chimaeroids, and that nerve relationships support the homologies proposed in Table
1.
Another way to judge the validity of these homologies is to consider what they
imply about the phylogenetic position of chimaeroids. With lips that are intermediate
in structure between those of ammocoetes and sharks, chimaeroids could not have
evolved from sharks, as some have claimed (Dean, 1906; Nelson, 1976; Maisey,
1984; 1986). Instead, chimaeroid ancestors must have evolved from earlier
Chondrichthyes, before Middle Devonian times (as suggested by Patterson, 1965;
Schaeffer &Williams, 1977; Schaeffer, 1981; and Young, 1982).Consistent with this
interpretation, many groups of Palaeozoic ‘holocephalians’ existed that definitely
were not sharks, but differed from sharks in having a short, subcranial pharynx, and
usually, holostyly and durophagy (e.g. chondrenchelyids, iniopterygians, cochlio-
ORIGIN OF JAWS
379
donts, Echinochimaera: Zangerl & Case, 1973; Zangerl, 1981; Lund, 1982; 1986;
Carroll 1988);and chimaeroids are thought to have evolved from one of these groups
(Patterson, 1992). If their ancestors originated before known sharks, it seems
reasonable to conclude that chimaeroids retain some primitive gnathostome
characters along with their obvious specializations. Along with their lips and
V,-innervated muscles, the following characters of chimaeroids can be considered
primitive: the nonsuspensory hyoid arch with pharyngohyal element; the rudimentary stomach (Dean, 1906); simple hypobranchial muscles lacking a coracoarcualis;
internal rectus muscle inserted anteriorly on the eye (Young, 1986: 51); a crus
commune in the otic labyrinth (Schaeffer, 1981: 51-52); and certain features of the
telecephalon (no central nucleus and no pallium bridging the two hemispheres:
Northcutt, 1977: 415).
lh ancestral lips and mouth. Based on the homologies presented above, Figure 26
reconstructs the lips and mouth of the jawless common ancestor of all living
vertebrates. The upper lips were well developed, although the condition in
chimaeroids and sharks suggests these lips were not as large as in ammocoetes.
Muscles ran from the braincase into the upper lips (as in ammocoetes and
chimaeroids).As already argued, the paired nostrils lay at the tip of the snout (which
matches the earliest fish in which nostrils can be identified, Sacabambasfvijanuzki, from
the Ordovician: Gagnier, 1989: 252). The mouth opening was circular and smaller
than that of the earliest known sharks (based on ammocoetes and chimaeroids). A
ring of oral cartilages lay directly behind the continuous lateral and lower lips, and
supported both the anterior margin of the mouth and some sensory tentacles. These
oral cartilages were not serially homologous to the branchial arches (not a
premandibular arch). Behind this oral ring, in the cheek, a buccal constrictor circled
the premandibular oral cavity (Fig. 26B). This constrictor graded posteriorly into the
superficial branchial constrictors around the pharynx. (Although it is most evident in
ammocoetes, an unmodified buccal constrictor muscle also occurs in embryonic
hagfish: Holmgren, 1946: 35). The anterior part of the buccal constrictor was
thickened into a distinct oral sphincb ( = elevator labialis ventralis of ammocoetes and
labialis posterior of Chimaera).
How did this jawless ancestor feed? The reconstructed oral structures seem well
suited for “feeding on semi-sessile soft-bodied invertebrate prey” on the ocean floor
(Gans, 1989: 248), where ingestion involved pushing the head against the prey and
forcing it into the oral cavity (Northcutt & Gans, 1983: 13). In this feeding act, the
oral sphincter would have squeezed the ring of oral cartilages to grasp the prey
animal, then the buccal and branchial constrictor muscles would have squeezed
(swallowed) the prey back to the oesophagus through peristalsis. No suction was
involved in ingesting and swallowing prey. The upper lips and tentacles would have
been tactile and gustatory structures, respectively, for detecting prey on the substrate.
The mobile upper lips could have draped over the prey, trapping it against the
sediment surface directly in front of the mouth, thereby facilitating ingestion.
Covered with tiny denticles (odontodes of Reif, 1982),this ancestor would have been
more mobile and wide-ranging than the more heavily armored osteostracans and
heterostracans. I picture it as nektobenthonic, actively swimming along the ocean
floor in search of food and stopping to rest only occasionally.
Is this reconstructed ancestor of the living vertebrates represented by any known
fossils? It would have lived in the Late Ordovician (Fig. l), but known fossils of
J. M
A
L
L
A
m
380
Ordovician vertebrates are either too fragmentary to allow a reconstruction of their
body form or else are heterostracan-like and therefore not ancestral (Darby, 1982;
Gagnier, 1989). Back in the Cambrian period - which may be too early to be
pertinent - 0dontogrihti.s omulus had a circular mouth opening surrounded by
uncalcified ‘teeth’ (Dzik, 1993),which might have grasped prey as my reconstruction
predicts. However, it is uncertain whether Odontogriphus was actually a chordate
(Aldridge, 1987: 23; Gould, 1989: 147).Conodont animals, pelagic and nektobenthic
vertebrates that originated in the Cambrian, fit my reconstruction but in only a
vague way. There is evidence that they were predators that grasped or speared prey
(Sweet, 1985; Purnell, 1993; 1995),but their grasping elements (conodonts)lay in the
pharyngeal region behind the eye and under the notochord, not in the pre-optic oral
cavity where my reconstruction predicts (Aldridge et al., 1993; Smith & Hall, 1993;
A
B
buccal constrictor
Figure 26. Lips and mouth of the proposed common ancestor of all living vertebrates; also see Figure 2E.
A, external view, but also showing some cartilages and the muscles in the uppr lip; B, view with the skin
and the snout removed, emphasizing the muscles around the oral cavity and pharynx.
ORIGIN OF JAWS
38 1
Sansom, Smith & Smith 1994; Gabbott et al. 1995).In conclusion, the reconstructed
ancestor has no fossil counterpart and must remain hypothetical.
By reconstructing the ancestor as a predator, I must abandon an earlier view that
ancestral adult vertebrates were suspension feeders (Mallatt, 1984a, by 1985).I now
accept the argument of Northcutt & Gans (1983) that only predaceous metazoans
evolved the type of distance receptors (e.g. eyes) that vertebrates possess. However,
evidence remains valid that the larvae of ancestral vertebrates were pelagic suspension
feeders that fed much as ammocoetes do: The tracts of feeding cilia and the endostyle
of ammocoetes are directly comparable to those in adult protochordates (Mallatt,
1984b: 262; Jefferies, 1986: 153). This concept of a suspension feeding larva that
metamorphosed into a predatory adult vertebrate also agrees with the ideas of
Northcutt & Gans (1983).
Evolution of the ammocoete condition
The oro-labial region of ammocoetes differs from the reconstructed ancestral
condition in three ways. First, the upper lip is enlarged, presumably having become
so when the ancestors of ammocoetes became burrowers (the ways in which
ammocoetes use their enlarged upper lip to sense and move through sand were
already discussed). Second, the premandibular oral cavity is enlarged, to hold the
velum that projects forward into this cavity.
The third derived feature in the oral cavity of ammocoetes is the ventral
longitudinal crest (Fig. 18A), which metamorphoses into the lingual apparatus
(‘tongue’)of adult lampreys. Many authors have suggested that the ancestor of all
vertebrates had such a lingual apparatus (Jollie, 1968; Hardisty, 1981: 37 1;Janvier,
1981; Jefferies, 1986: 160; Forey & Janvier, 1994), but I disagree, considering it
unlikely that gnathostomes would have lost such a large structure without a trace.
Furthermore the oral cavity (prebranchial fossa) of osteostracans was too small to
have held a large lingual apparatus (Goodrich, 1930~).I propose that the lingual
apparatus evolved in the adult ancestors of extant agnathans as an appendage that
helped pull worms into the mouth and back through the oral cavity - because that
is how hagfish use this apparatus and the associated dental plates (Dawson, 1963;
Mallatt, 1985: 66). The lingual apparatus of adult lampreys pulls and slices food, and
its anatomy suggests it is homologous to that of hagfish (Yalden, 1985).
Evolution o f the gnathostome and chondrichthyan conditions
Judging from the many resemblances between the oro-labial structures of
ammocoetes and chimaeroids, the evolution of jaws had little effect on the external
anatomy of this premandibular region (Fig. 16A-C). That is, in the earliest
gnathostomes, the cheeks still reached far forward and the mouth opening was not
enlarged (Fig. 16C). However, the mouth opening had attained its lateral corners,
reflecting the fact that it now closed in an up-and-down bite, no longer by sphincter
action. Furthermore, the &nctions of the oro-labial structures had begun to change:
Judging from both chimaeroids and sharks, the earliest gnathostomes could protrude
and then retract their cheeks during suction feeding, and the upper and lateral lips
now served to round the mouth opening during the expansive phase of the feeding
strike.
Evolution ofsharks. Early elasmobranchs began to chase down large, pelagic prey, and
the gape of their mouth enlarged to fit this larger prey (Fig. 16D). To allow this, the
382
J. MALLATT
lateral corner of the mouth migrated far posteriorly, and the cheek folded into a deep
labial pouch as a buccal membrane. Simultaneously, the most anterior part of the
upper lip flattened to avoid blocking prey entering the mouth (although the posterior
part of this lip remained as the lateral fold). In essence, the premandibular mouth
structures became smaller to avoid interfering with the capture of large prey by the
jaws. Incidentally, independent enlargements of the gape must have occurred in the
ancestor of acanthodians and Osteichthyes, and in the most highly predacious of the
arthrodire placoderms.
Evolution ofchimaeroids. Are the small gape and large cheeks of chimaeroids truly
primitive, as proposed here, or did these traits evolve secondarily? Theoretical
considerations indicate they could be retained primitive traits: Denison (196 1)
proposed that the enlarging gape and jaws of early sharks was responsible for the
modification of their hyoid arch into a thick brace between the jaws and braincase.
Because the hyoid arch of chimaeroids is not modified like this, the relatively small
gape and jaws of these animals should be primitive. By this reasoning, chimaeroid
feeding must echo a stage after the evolution of jaws but before large, evasive prey
were chased down and swallowed whole. Indeed, chimaeroids feed mainly on slow
invertebrates such as molluscs, crabs, echinoids, polyps, shrimps, and amphipods
(Dean, 1906: 20; Halstead & Bunker, 1952; Sathyanesan, 1966; Ribbink, 1971;
Young, 1981). Although their diets contain many hard items, and their jaws and
teeth obviously are modified for forceful shearing or durophagy (Patterson, 1992;
Didier, Stahl & Zangerl, 1994), chimaeroids otherwise retain the benthic feeding
mode of ancestral vertebrates.
Ou@oup comparison
Are the lips and mouth structures of other jawless vertebrates and chordates
consistent with those reconstructed for the ancestor of living vertebrates?
Adult lampreys. The feeding ecology and oro-labial structures of adult lampreys seem
to be highly specialized. It is proposed that their parasitism on fish evolved through
a multi-step sequence. After the ancestors of extant agnatha evolved a lingual
apparatus to help grasp and slice benthic invertebrates, the anaspid ancestors of
lampreys used this apparatus to cut and scrape films of algae from rocks and the
sediment surface (Gilmore, 1992). These pre-lampreys also scraped mucous films
from the skin of bony fish, and finally, sliced flesh from such fish. (This sequence is
a modification of one I presented previously: Mallatt, 1984b; 1985.) Structurally, the
premandibular oral cavity elongated to accommodate the lingual apparatus in its
floor, and the upper lip expanded into a sucker (oral disc) for attaching to rocks and
prey fish. Beyond this, detailed homologies with gnathostomes and even with
ammocoetes are uncertain. So many larval cartilages and muscles de-differentiate
during lamprey metamorphosis that one cannot determine how they relate to the
adult structures that appear later (Hardisty, 1981; Hardisty & Rovainen, 1982). This
is one reason why adult lampreys receive so much less consideration than
ammocoetes in this paper.
HagFrh. Hagfish feed on benthic worms and other invertebrates, and they scavenge
the remains of dead fish on the ocean floor (Shelton, 1978). The oral cavity is long,
as in lampreys, and it contains the large dental plates of the lingual apparatus. Unlike
ORIGIN OF JAWS
383
lampreys, hagfish lack an oral disc, and the snout region containing the nasal passage
is elongated (Hardisty, 1979).
Some oro-labial structures of hagfish seem to match those of the reconstructed
ancestor (Fig. 27). As in ammocoetes and sharks, the mouth opening is supported by
a ring of oral cartilages - called labial cartilages by Ayers &Jackson (1900) and
coronary cartilages by Marinelli & Strenger (1956). As in ammocoetes, these
cartilages support oral tentacles. Muscles around this cartilage ring could represent
the primitive oral sphincter (m. coronarius and m. basitentacularis), whereas muscles
in the walls of the long oral cavity could represent the ancestral buccal constrictor
(mm. levator and protractor cartilaginis basalis: Lindstrom, 1949: 320; Marinelli &
Strenger, 1956). It is of interest that the oral cartilages and tentacles are well
developed in the 300-million-year-old fossil hagfish, Myxinhlu siroka (Bardack,
1991).
An upper lip may exist in hagfish as a cornual cartilage and the associated
cornuosubnasal muscles (Fig. 27). These structures project laterally from the snout
but are hidden from surface view under loose skin. By this interpretation, the cornual
cartilage is homologous to the rostro-dorsal plate of ammocoetes (Parker & Haswell,
1962: 200). In support of this, both of these skeletal structures attach to the anterior
braincase under the nasal capsule, and both lie directly dorsal to a large, horizontal
branch of the trigeminal nerve that runs to the tip of the snout (V, in ammocoetes
and ramus muscularis anterior externus in hagfish: Marinelli & Strenger, 1956:
106).
Amphioxus. Homologies in the mouth region of amphioxus are more questionable, but
they are often discussed (Pollard, 1894; Goodrich, 1930a: 448; Ayers, 1931; Luther,
1938: 47 l), so they should be considered in the present context. As shown in Figure
cornual
cornuosubnapal
cartilage
coronarius
muscle
muscles
\
I
labidcoronary
uutilage around
mouth opening
I
O h
cavity
\
\
d
d plate
Figure 27. Anterior part ofa hagfish (MyxitUgluhosu).As explained in Table 1, the labelled cartilages and
muscles may be homologous to structures in ammometes and Chondrichthyes. (Based on figure 10 in
Holmgren, 1946, and figure 130 in Marinelli & Strenger, 1956.)
384
J. MALLATT
17, the lateral walls of the oral cavity anterior to the velum are formed by an oral
hood, which should be homologous to the lateral walls of the oral cavity of
ammocoetes and to the buccal membrane of sharks. To avoid a point of confusion,
the oral hood of amphioxus is not homologous to the oral hood of ammocoetes (the
upper lip) - amphioxus has no upper-lip homologue at all. In amphioxus, a sieve
of oral tentacles projects anteriorly from the oral hood. These tentacles have the same
relative location and function (stopping entry of large food particles) as the oral
tentacles of ammocoetes, and the two could be homologous to one another, and also
to the oral tentacles of hagfish. Each tentacle in amphioxus contains a rod of
cartilage, and the bases of these tentacular cartilages form a U-shaped hoop around
the free margin of the oral hood. This hoop would be homologous to the lateral
mouth plates of ammocoetes and the labial/coronary cartilages of hagfish, all of
which support tentacular cartilages. Peri-buccal muscles (Drach, 1948) lie against the
bases of the tentacular cartilages of amphioxus and encircle the oral hood; therefore,
these muscles may correspond to the ancestral oral sphincter (or else to the basalis
tentacularis of ammocoetes). The possible homologies between amphioxus and
vertebrates are included in Table 1.
Ostrucodm. This section focuses on the mouth structures of heterostracans and
osteostracans, but galeaspids will be discussed briefly. Galeaspids had an enlarged
premandibular oral cavity and a nasohypophyseal opening like that of hagfish
(Janvier, 1984). Additionally, although most galeaspids had an unmodified
mandibulohyoid grU pouch and therefore no velum (Fig. 13C), at least one species
had an enlarged space behind the eye and mandibular arch that could have housed
a pumping velum (Duyuna-spkpuoyangenris;
see ‘dp2’ and ‘dp3’ in figure 4D ofJanvier,
1984). For these reasons, I relate galeaspids to the living agnathans in Figure 1A
(although other features, such as perichondrial bone and a large lateral head vein,
may unite them with osteostracans: Wang, 1991; Young, 1991;Janvier, 1993).
In heterostracans (Fig. 28), the rostral and lateral region of the snout may
represent an ammocoete-like upper lip. Behind this lay the premandibular oral cavity
(Fig. 28A), which cannot be reconstructed in detail because much of its roof
apparently was cartilaginous and is not preserved in the fossils. Even so, the mouth
region provides clues to the feeding mechanism. In the main groups of
heterostracans -cyathaspids, pteraspids, and Sucabumbaspts- a row of narrow,
movable oral plates projected forward from the inferior border of the mouth
(Denison, 1964; Soehn & Wilson, 1990;Janvier & Blieck, 1993).All surfaces of these
plates were ridged except their posterior dorsal surface, suggesting the latter was an
attachment site for a muscle that lifted the plates to scoop benthic invertebrates into
the mouth (Denison, 1961; Tarrant, 1991: 432). This interpretation fits the idea that
ancestral vertebrates fed on slow, benthic prey. The oral plates would have been
lifted by the ancestral oral sphincter (elevator labialis ventralis) (also see Stensio,
1958).
In osteostracans, the anatomy of the oral cavity is interpreted as follows (Figs 29
and 13B).The most anterior ridge on the roof of the head shield reaches down to the
posterior margin of the mouth opening, so this ridge must represent the lateral
mouth plate of ammocoetes-the ancestral oral cartilage. Behind this ridge lies a
small oral cavity (prebranchial fossa ofJanvier, 1993: 165), followed by a ridge that
represents the external mandibular arch and marks the proposed location of the oral
valve. Posterior to this is the mandibulohyoid gill pouch, which has the first external
ORIGIN OF JAWS
385
gdl opening plus impressions of gill structures and the facial nerve (VII). Returning
to the front of the animal, the part of the head shield anterior to the oral cartilage
must correspond to the upper-lip cartilage, or rostro-dorsal plate of ammocoetes.
The ceiling of this upper lip has paired supraoralfossu, proposed attachment sites for
the elevator labialis ventralis muscles (Janvier, 1985). Recall that in ammocoetes
these muscles likewise attach to the upper lip (i.e. to the rostro-dorsal plate at the
suborbital processes). The supraoral fossae lie just medial to the groove for V,, as do
the elevator labialis ventralis muscles of ammocoetes.
This interpretation of osteostracan anatomy agrees with that of several previous
authors (Allis, 1931; Lindstrom, 1949; Moy-Thomas & Miles, 1971) in identifjmg
the first pocket with impressions of gill structures as the mandibulohyoid gdl pouch.
It demands that the facial nerve innervated the entire mandibulohyoid pouch as well
as the hyoidean gdl (Janvier, 1985).That would match the condition in gnathostomes
(Goodrich, 1930a; Hyman, 1942: 469), but not lampreys, where VII supplies only
the hyoidean gdl (Alcock, 1898). Essentially, it would mean that the branchial nerves
of osteostracans had both pretrematic and postrematic branches as in gnathostomes,
whereas pretrematic branches do not exist in living agnathans. This proposal is not
far-fetched, however, given that osteostracans are related to gnathostomes (Fig.1).
My reconstruction differs from that of Janvier (1985), who placed both the
position ofmandibular arch
A
cavity
B
Figure 28. Heterostracans. A, lateral view of PterapL (Phhp&uspis dcprwJa of Stensio). Notice the oral
plates. The stippled region is the oral cavity (the region anterior to the impressionsof the first gdl pouch),
and it seems too small to have held a large, pumping velum; B, ventral view of the mouth of another
Pterapis species (,?&inu.spir of Stensio). The oral plates could be raised, and an oral spincter may have
been present to perform this action (although the precise location of this muscle is speculative).
Illustrations modified from figures 137 and 143A in Stensio (1958).
J. MALLAl'T
386
external hyoid and mandibular arches on the second ridge back (that is, on the 'ridge
for external mandibular arch' in Fig. 29B). His reconstruction was said to be based
on ammocoetes, where the external hyoid and external mandibular (velar)bars are
close together. On the contrary, these two bars are far apart in the dorsal half of the
ammocoete pharynx, separated by the velohyoideus muscle and the hyoidean venous
sinus (personal observation on sectioned Petromyzon marinus). Thus, there seems to be
no basis for reconstructing two bars on a single ridge on the pharyngeal roof of
osteostracans.
If my interpretation of osteostracan anatomy is correct, it means that their
horizontal mouth opening was not the true vertebrate mouth opening, but rather the
opening formed by the edges of the upper lip (Fig. 29C). The true mouth opening lay
between the ridges for the oral cartilages and was vertical. (Incidentally, this parallels
1I
A
B
C
rid efor
OJcartilage
\
(and site of oral valve)
Figure 29. The osteostracan Norsehpisgrocia1i.s. A, dorsal view of the fish, for orientation; B, right half of
the mouth and anterior pharynx; C, enlargement of the snout region from B, showing the two different
mouth openings. Although these drawings have been modified from figures 51A and 73A in Janvier
(1985),the interpretation of the branchd arches and pouches matches that of Lindstrom (1949;also see
fig. 2.5 in Moy-Thomas and Miles, 1971).
ORIGIN OF JAWS
387
the condition in adult lampreys, whose oral hood also forms the functional mouth
opening.)
The feeding mechanism of osteostracans is more dimcult to reconstruct than that
of heterostracans, because the precise shape of the mouth opening is known in only
a few species (see fig. 10 in Stensio, 1968, and fig. 18 in Janvier, 1985). In some, this
opening was just an oval hole, but in others oral plates lay just behind it (Robertson,
1970; Janvier, 1985: 46). In at least one species (Hirella gucdis), these plates were
joined by a hinge line to the ventral dermal cover, and could have been lifted up to
‘bite’ against the anterior rim of the head shield (P.Janvier, pers. comm.). Therefore,
some osteostracans may have scooped up benthic invertebrates (stream-dwelling
insect larvae?), like heterostracans did. However, the mouth opening was so small
that only tiny prey could have been ingested. (An alternate view, based on the large
size of the pharynx compared to the oral cavity, is that osteostracans were suspension
feeders or benthic detritivores: Mallatt, 1984b).
Little has been said about thlodonts in this paper, despite their great importance,
because few whole-body specimens are preserved. However, enough is preserved to
suggest that their oral and pharyngeal regions fit the structural pattern identified in
the other ostracoderms and chondrichthyes (Fig. 13D). That is, some thelodont
specimens show a ring-shaped oral cartilage (Stetson, 1931; Turner, 1993), then a
premandibular oral cavity, an impression for the mandibular arch, and a
mandibulohyoid gill pouch (with the latter just behind the eye: Wilson & Caldwell,
1993). This is especially significant because thelodonts are most closely related to
gnathostomes (Turner, 1985).
To summarize Section 3, many agnathans and gnathostomes share a set of orolabial structures (Fig. 1C). From anterior to posterior, these are an upper lip, mouth
opening with oral cartilage and oral sphincter, premandibular oral cavity, and the
mandibular arch (also see Jollie, 1968). Conservative features of the lips, muscles,
nerves, and cartilages around the mouth bridge the otherwise vast gulf between
jawless and jawed fish. By considering only the skeleton and chasing the red herring
of ‘premandibularbranchial arches’, past studies of jaw origins overlooked important
homologies in the oral soft structures.
The above considerations argue against the classical theory of the origin ofjaws,
i.e. that the mandibular arch enlarged to grasp prey during feeding. The problems
are that the mandibular arch lay far back, and the ancestral oral structures in front
of it (Fig. 1C) would have interfered with its ability to seize prey. Furthermore, these
oral structures already captured and grasped prey during feeding, offering no
obvious reason for the mandibular arch to adopt this function. A new explanation for
the origin of mandibular jaws seems necessary.
THE PROTOCHORDATE-TO-GNATHOSTOMETRANSITION
VENTILATION AND THE ORIGIN OF JAWS
The preceding sections have established substantial similarities between jawless
vertebrates and gnathostomes, and many new homologies have been proposed. Now
this information will be related to the evolution ofjaws. I will argue that the changes
within this evolutionary sequence were associated, at least initially, with ventilatory
changes (and only later with feeding changes). It is likely that these changes occurred
388
J. MALLA'IT
through a series of stages, each of which addressed new metabolic demands and took
advantage of previously evolved structures.
Earliest vertebrate
Protochordates such as amphioxus and tunicates have low metabolic rates and a
sedentary lifestyle (Courtney & Newell, 1965; Alexander, 1981). During the
transition to vertebrates, activity levels began to increase, probably due to a switch
from suspension feeding to predation (Gans & Northcutt, 1983; Gans, 1989; 1993;
Purnell, 1995). Changes to more active lifestyles have been proposed as the basis for
the appearance of many vertebrate characteristics (Jollie, 1973, 1982a; Northcutt &
Gans, 1983; Ruben & Bennett, 1987),including gdls and muscular ventilation (Gans,
1989). Extending this idea, I propose that additional adaptations to increased
metabolic demands occurred in ventilatory structures and continued to evolve
throughout the first great radiation of jawless and jawed vertebrates. The following
scenario is provided (Fig. 30), beginning with the earliest vertebrates possessing a
relatively low metabolic scope.
Common ancestor of all living uertebrates
Judging from shared features of sharks and ammocoetes, their common ancestor
ventilated as follows. Expiration was an active process effected by a peristaltic
contraction of the branchial constrictor and interbranchial muscles, which pushed
water across the gills (this was the pressure pump). During expiration, the thin flaps
of the oral valve were pushed shut, preventing reflux through the mouth. Inspiration
was strictly passive, brought about by recoil of the unjointed external and internal
branchial arches. Through this recoil, the pharyngeal lumen and gdl pouches
enlarged to draw in water from the outside, and the parabranchial chambers
enlarged to suck water laterally across the gills (the latter was the suction pump).
This common ancestor lacked a pumping velum. Its premandibular mouth and
lips were used for feeding on slow, soft benthic prey. It is illustrated in Figures 2, 3,
15A, and 26.
According to Northcutt & Gans (1983: 20), ancestral vertebrates became
progressively more active and effective predators throughout their early history. If so,
both their basal metabolic rate and their capacity for prolonged activity would have
increased. Selection would have favoured an increase in the area of the gdlrespiratory surface. The increasing number and density of respiratory lamellae, in
turn, increased resistance to ventilatory flow, demanding stronger ventilatory
pumps.
Ancestor of living agnathans
The pumps were strengthened in different ways by different lineages of
vertebrates. On the one hand, the ancestors of ammocoetes and hagfish evolved a
ORIGIN OF JAWS
389
powerful, pumping velum, which allowed these burrowers to pump against the
resistance of fine sediment, as well as across increasing numbers of respiratory
lamellae. This strategy proved evolutionarily limiting, however, in that it strengthened the pressure pump without fundamentally changing the suction pump.
Therefore, apathans cannot generate the strong suction forces that jawed fish use to
draw prey into the mouth (Mallatt, 1984b). Because the oral cavity held a large
velum and/or a lingual apparatus, this premandibular region enlarged.
ELASMOBRANCHS
-larger prey
OSTEICHTHYES
-larger prey
ACANTHODIANS
-small prey
CHIMAEROIDS
-strong bite,
crushing and
slicing
PLACODERMS
-strong bite,
s1icing
hyoid braces jaw
---J--------_-____-fast, pelagic prey
gape , hyoid
braces jaw
(some)
slow, benthic prey
5. EARLY GNATHOSTOME (feeding jaws)
-jaws first used to grasp prey
-suction feeding
-new mouth (postmandibular pharynx)
-aphetohyoid
-last stage to take slow, soft, benthic prey
en-arging
jaws
4. LATE PRE-GNATHOSTOME (ventilatory "jawsH)
-now could close and open the mouth during
heavy ventilation
-enlargement of the mandibular arch and its
muscles for this purpose
3. EARLY PRE-GNATHOSTOME
-stronger ventilation; active inspiration
-new ventilatory muscles (s.g., the
hypobranchials)
-jointed, mobile internal arches
LIVING AGNATHANS
-pumping velum
-enlarged oral
cavity, with
a "tongue"
2. COMMON ANCESTOR OF ALL LIVING VERTEBRATES
-active expiration, passive inspiration
-unjointed internal and external branchial
arches
-oral valve but no pumping velum
-ate slow, soft, benthic prey
-old mouth (premandibular oral cavity)
IIncreasing
activity,
selection for stronger
ventilatory pumps
i
1. EARLIEST VERTEBRATE
-gills present, muscular ventilatory pump
-lowest metabolic and ventilatory rates
-incipient predator
Figure 30. Summary of the functional stages in the evolution of gnathostomes.
390
J. MALL4lT
Earb pre-gnathostome
In the pre-gnathostome line of vertebrates, by contrast, both of the ventilatory
pumps were strengthened. This was done by subdividing and enlarging the muscles
to the internal branchial arches, by strengthening the arches themselves, and by
utilizing the potential for these arches to move extensively within the pharynx. New
expiratory muscles (interarcuals and adductor branchialis) strengthened the pressure
pump by pulling the arches and the arch segments closer together to decrease
pharyngeal volume. New inspiratory muscles (hypobranchials) pulled these arch
elements apart during forceful inspiration, increasing pharyngeal volume and greatly
strengthening the suction pump. Although such inspiratory muscles are not active
during normal quiet ventilation (Hughes, 1974), they allow gnathostomes to produce
strong suction forces and to increase ventilatory flow rates, as needed. Several
previous authors have emphasized the importance of inspiratory hypobranchial
muscles in the origin of gnathostomes (Hughes & Ballintijn, 1965; Lessertisseur &
Robineau, 1969, 1970).
In this early pre-gnathostome, ventilation was stronger with a capacity of active
inspiration as well as expiration to meet increased metabolic demands. New
ventilatory muscles had appeared, the branchial arches were jointed, and the robust
internal arches predominated over the persisting external arches. This stage is shown
in Figures 10 and 16A.
Late pre-gnathostom (ventilutory jaws?
As the ventilatory pumps of pre-gnathostomes became more powerful, new
mechanisms evolved for closing and opening the mouth. The ancestral oral valves,
while adequate for preventing reflux of water during quiet ventilation, would have
leaked during powerful, rapid ventilation. More specifically, these passive valves
would have everted under the strain of increasing expiratory pressures in the
pharynx, and their inertia consistently would have caused them to lag behind the
rapid pressure changes. To keep water from leaking out of the mouth, the first
branchial adductor (adductor mandibulae) enlarged and gained the ability to close
the mouth opening during each expiratory phase, by sharply flexing the
ceratomandibular (lowerjaw) on the epimandibular (upperjaw). In short, a urntilatory
jaw mechanism evolved (Fig. 16B). Consistent with this idea, many living sharks and
bony fish close their jaws during expiration (Hughes & Ballintijn, 1965: 37 1; Hughes,
1974).As the jaw-closing muscles enlarged, the coracomandibular and coracohyoid
muscles gained the ability to re-open the mouth quickly during forceful inspiration
(Motta, Hueter, & Tricas, 1991). Concomitantly, these hypobranchial muscles
enlarged further. The mandibular branchial arch became more massive to withstand
the increased pulling forces produced by the mouth-closing and mouth-opening
muscles.
Acknowledgement must be given to Wahlert (1970) and Reif(1982) for an earlier
version of the idea that jaws evolved for ventilation. However, whereas I emphasize
the role of jaw movements in preventing leakage, those authors saw the ventilatory
jaw as helping to push and pull water into the pharynx. Furthermore, they proposed
that the mandibular arch originally stiffened the rim of the mouth opening, a role
that I attribute to the premandibular oral cartilage.
ORIGIN OF JAWS
391
In late pre-gnathostomes, once the mandibular arch and its musculature became
a bit larger than the other arches posterior to it, these mandibular structures
automatically would have performed an ‘anchor’ function, as they do in dogfish
sharks (Hughes & Ballintijn, 1965). That is, inertia caused this more-massive arch to
lag behind the other arches during ventilatory movements, thereby stretching
fibroelastic membranes between the successive arches during expiration, with the
subsequent elastic recoil strengthening the force of inspiration. This recoil action is
aided by tonic activity of the adductor mandibulae. Selection to improve this
beneficial anchor function, in turn, would have led to a hrther enlargement of the
mandibular arch and its adductor muscles.
Jaws that evolved under selective pressures to serve strong ventilation offered the
opportunity to close and open the mouth forcefully. This late pre-gnathostome stage
is illustrated in Figure 31A as well as 16B.
Ear& gnathostome fieding jaws)
The threshold to the gnathostome condition had been reached - all within a
ventilatory, not a feeding, framework. However, with the jaw mechanism now in
place, feeding changes would have followed immediately. The jaws could clamp shut
to catch and hold prey. Large, strong prey that previously squirmed out the mouth
could now be retained and eaten. Furthermore, it no longer was necessary to press
the prey against the substrate to ingest it, because the strong suction produced by the
hypobranchial muscles could draw prey into the mouth from a distance. Therefore,
the descendants of early gnathostomes could chase down mobile prey for the first
time, and leave the confines of the benthic environment. Any swimming animal in
the water column that could be overtaken and bit or sucked into the mouth became
a potential meal. Once it took on a feeding role, the jaw mechanism became still
more powerful and enlarged again (Fig. 16C).Now, gnathostomes were poised to rise
rapidly to the top of the food chain, catching ever larger, faster prey. The early
gnathostome is illustrated in Figures lB, 16C, and 31B.
Although suction feeding based on powerful pharyngeal expansion is more highly
developed in ‘advanced’ gnathostome fish than in ‘primitive’ ones (Lauder, 1980b,
1982; Frazetta & Prange, 1987; Moss, 1977; Wu, 1994), several considerations
indicate that suction was an essential part of aquatic prey capture in the earliest
gnathostomes. First, all gnathostomes have the suctorial hypobranchial muscles.
Second, chimaeroids use suction feeding (personal observations), and it already has
been argued that chimaeroids resemble early gnathostomes in key aspects of their
feeding. Third, it is impossible to capture pelagic or fast prey unless suction is
produced. When a predatory fish swims at a prey animal, the prey is deflected away
by streamlines emanating from the fish’s head; the fish must generate suction to
overcome such deflection and direct the prey into the mouth (Lauder & Clark, 1984;
Lauder, 1985).
During this early gnathostome stage, the ancestral oral cavity (‘old mouth’) was
reduced and a new mouth appeared (Figs 1C and 3 1). As the enlargingjaws took on
a feeding function, they rotated into a horizontal position to brace against the
braincase (so they would not shear during prey capture) and grew forward to reach
the tip of the snout (so their grasping anterior margins could encounter prey before
any other part of the head). This anterior extension reduced the part of the ancestral
J. MAUATT
392
A LATE PRE-GNATHOSTOME
B.EARLY GNATHOSTOME
psardobmch
ORIGIN OF JAWS
393
oral cavity in the medial ‘symphseal’ regions to a functionless slit between the lip and
jaw of gnathostomes. Laterally, the side walls of this old mouth remained, and persist
in Chondrichthyes as premandibular cheeks or buccal membranes that project
forward to round the mouth opening during suction feeding.
If the ‘old mouth’ of gnathostomes is the premandibular slit separating the lips and
cheeks from the jaws, what is their ‘new mouth’? This is the region directly behind
the jaws that is traditionally called the mouth, oral cavity, or buccal part of the
buccopharyngeal cavity (Figs 3 1C and 1C). Actually, it is not a mouth at all but the
anterior part of the pharynx. Its innervation proves this. Whereas the mucosa lining
the true, premandibular oral cavity of lampreys and hagfish is innervated by the
that of the postmandibular oral cavity of sharks and bony fish
trigeminal nerve 0,
is innervated by the facial (VII), an undisputed pharyngeal nerve; and the V/VII
boundary lies approximately at the jaw margins (Cole, 1896; Norris & Hughes, 1920;
Allis, 1923: 213-214; Daniel, 1928: 242; Goodrich, 1930a: 752; Hyman, 1942:
468469). Therefore, in early gnathostomes, when the mandibular arch pushed
C. SHARK (SQUALUS)
adductor
mandibulae,
/!Ah i
palatoquadrate-
Figure 31. Evolution of the new mouth. A and B show the transition in sagittal section. A, late pregnathostome. B, early gnathostome. As the ventilatoryjaws took on a feeding function, they rotated and
grew forward (see the large arrow in Part A). This narrowed the ancestral oral cavity (old mouth) in front
of them and formed a new mouth from the pharynx behind them. Sharp dentides on the medial margins
of the internal branchial arches later evolved into the teeth (see fig. 77 in Smith, 1937, and Van der
hunthk, shows the new
Brugghen & Janvier, 1993). C, a cut-open view of the oropharynx of ~ u a u
mouth as well as the slit-lie remains of the old mouth. In ammocoete lampreys, the homolopes of the
old mouth and new mouth are the oral cavity and the part of the pharynx directly behind the velum,
respectively, as shown in the sagittal section in Figure 2B.
394
J. -‘IT
forward to squeeze the old mouth into a slit, it pulled the pharyngeal mucosa along
behind it, forming a new mouth.
But why, ultimately, did a new mouth evolve? That is, why did new mandibular
jaws enlarge and assume the prey-grasping hnction when the ancestral oral
cartilages and oral sphincter were already acting to grasp prey? Why not simply
enlarge these ancestral grasping structures to form the jaw mechanism? The answer
is simple: jaw evolution was a ventilatory phenomenon, and the oral sphincter
muscle was not ventilatory in function; it was not ‘wired’ to the parts of the brain that
closed the mouth at the s t a r t of each ventilatory cycle as the adductor mandibulae
behind it was. The uentilatoly mouth-closing and mouth-opening device became the
jaws.
?he gnathostome radiation
As mentioned, the appearance of suction feeding and biting jaws was an adaptive
breakthrough that led to an explosive radiation of gnathostomes in the Silurian (see
the top of Fig. 30). What was the nature of that radiation, and how does it relate to
the known groups of Palaeozoic gnathostome fish? My scenario predicts it involved
three basic changes in feeding ecology: (1) a transition from benthic to pelagic
predation; (2) the capture of more mobile prey; (3) the capture of larger prey. By this
interpretation, chimaeroids (and other ‘holocephalians’)and most placoderms never
made the changes away from the ancestral benthic habitat and slow prey, yet these
groups evolved powerful slicing and crushing bites very early in gnathostome history.
The ancestors of known elasmobranchs and bony fish, by contrast, underwent all
three changes and became voracious predators on large, fast pelagic prey by the
dawn of the Devonian period. In modern, ecomorphological terms these preelasmobranchs and osteichthyeans shifted from pure suction feeding toward ram
feeding (Norton and Brainerd, 1993), although it must be emphasized that ram
feeders still use suction to draw in prey. Acanthodians were similar to bony fish, but
took smaller prey. (These interpretations of how Palaeozoic fishes fed are based on
Moy-Thomas & Miles, 1971.).
Evaluation ofthe scenario
As indicated in Figure 30, my scenario demands that the hyoid arch did not
suspend the jaw in early gnathostomes, and the hyoid suspension evolved
independently in elasmobranchs, acanthodians/Osteichthyes, and certain placoderms. That is, the hyoid became attached to the skull three different times. In
support of this, the relation of the hyomandibula (ceratohyal)to the lateral head vein
and hyomandibular nerve at the skull’s otic region differs between all three fish
groups (Goodrich, 1930a: 417; de Beer, 1937: 410-411; Miles, 1971: 201; Young,
1986: 33-47; Schaeffer, 1981: 59). This high degree of convergence is easily
explained Because a suspensory hyoid is an adaptation to an enlarging gape and
large prey (Denison, 196l), it should have evolved in every early gnathostome group
that adopted such a feeding strategy.
The recent palaeontological literature has been critical of the above interpretation,
claiming instead that the hyoid was primitively suspensory, the spiracular pouch was
ORIGIN OF JAWS
395
never a gdl pouch, and the mandibular and hyoid arches were never ventilatory
(Reif, 1982: 347; Gardiner, 1984: 241; Maisey, 1984; 1989; Forey &Janvier, 1994).
This criticism is understandable, because past studies had wrongly assigned a
nonsuspensory hyoid (‘aphetohyoid’ theory) to acanthodians, all placoderms, and
some fossil sharks (Watson, 1937; see discussion in Maisey, 1989). However, errors
of application are not grounds for rejecting a theory. Nor is the absence of
aphetohyoid gnathostomes from the known fossil record, for my scenario confines
this aphetohyoid stage to the Ordovician and Silurian, a time from which almost no
complete gnathostomes of any sort are known. Actually, the aphetohyoid theory is
well supported by the many groups of ostracoderms that had a complete
mandibulohyoid pouch and gdl opening, plus widely-separated mandibular and
hyoid arches (Fig. 13). Additionally, the classical neontological evidence for a
respiratory origin for the mandibulohyoid pouch remains valid: The embryonic
arteries (Goodrich, 1930a: 5 14) and pretrematic and postrematic nerves (Table 2 in
Northcutt & Bemis, 1993) of this pouch resemble those of the typical gdl pouches.
Modern developmental studies further strengthen the case, indicating that the
mandibular and hyoid arches resemble the first typical arch behind them in their
Hox-gene expression patterns, relation to rhombomeres, their neural crest and
somitomere contributions, and the associated epibranchial placodes (Noden, 1991;
Gilland & Baker, 1993; Larsen, 1993: 368). The theory that the jaws and hyoid arch
once were typical respiratory arches remains strong.
But on a more basic level, does it make sense to claim that the feeding jaws of
vertebrates evolved primarily for ventilation? Functional studies have shown that the
act of feeding in aquatic gnathostome fish is an exaggerated ventilatory cycle
(Lauder, 1983; 1985). Prey capture is effected by opening the mouth and producing
suction, as in forced inspiration; then the jaws close on the prey and water is pushed
out the gdl openings, as in strong expiration. The same pharyngeal muscles contract
during the compressive phase of prey capture as during ventilatory expiration, and
in the same anterior-to-posterior sequence (Hughes & Ballintijn, 1965; Lauder,
1983). Even swallowing is simply a series of repeated inspiratory and expiratory-like
actions that move the prey back to the oesophagus (buccal manipulation: Lauder,
1983). Evidentally, feeding in jawed fish is a stereotyped ventilatory act that was
secondarily superimposed onto some other, ancestral feeding mechanism. Viewed
this way, the distinctive aspects of gnathostome feeding indeed could have evolved
for ventilatory reasons.
Is the present scenario supported by any known fossil gnathostomes ? Stahl(l980)
found that the jaws of some Palaeozoic iniopterygian Chondrichthyes were just
slightly enlarged epibranchial and ceratobranchial segments. These were weak,
fragde jaws, with tiny teeth, and Stahl suggested that they represented the primitive
gnathostome condition. Similarly, the jaws of primitive placoderms were covered
with tiny denticles that had not evolved into teeth (Reif, 1982: 336). Therefore, basal
Chondrichthyes and early placoderms might represent the stage in the scenario
when ventilatory jaws were just starting to become feeding jaws.
CONCLUSIONS
(1) This study addressed the origin of jawed vertebrates by re-examining structural
homologies among lampreys, sharks, and other vertebrates, and also by
396
J. MALLKIT
including new functional information. It considers soft structures as well as
skeletal and palaeontological data. It revives the concept of the cyclostomes
(lampreys and hagfish as a natural group) and argues that agnathans and
gnathostomes are more similar than is usually realized.
(2) The gills of lampreys and gnathostome fish are similar in structure and are fully
homologous to each other. However, the internal branchial arches were lost
from lamprey gdls, whereas these arches enlarged and became more complex in
the gdls of pre-gnathostomes, along with the associated ventilatory muscles. This
reflected a strengthening of the expiratory and inspiratory pumps for ventilation,
and it was an early step toward the evolution of jaws.
(3) The hypobranchial muscles of gnathostomes, which produce forceful inspiration, evolved from two sources: (i) the coracomandibular and coracohyoid
muscles evolved from myotomes; and (ii) the coracobranchialsevolved from the
interbranchial muscles. The coracobranchials originally attached to the fibrous
pericardium below the gills, later migrating back to the coracoid bar of the
pectoral girdle.
(4) Although the anterior region of the pharynx differs considerably between sharks
and lampreys, enough similarities were found to allow reconstruction of the
ancestral condition. Ancestrally, the hyoid and mandibular arches were
separate, ventilatory arches. Sharks are conservative in retaining a first gill (the
pseudobranch in a spiracular pouch). In lampreys, by contrast, the first gill
evolved into a pumping velum, which receives constrictor musculature from the
lateral wall of the pharynx and strengthens expiration in the larva. Unlike
lampreys and hagfish, the ancestors of gnathostomes never had a velum nor an
oral ‘tongue’ apparatus.
(5)The oral valve on the jaws of Chondrichthyes is homologous to the medial flap
of the velum of larval lampreys. This valve is an important landmark in the
anterior pharynx.
(6) During the evolution of gnathostomes, the internal mandibular branchial arch
enlarged to form the jaws. Its jaw-closing adductor musculature apparently
migrated from the medial to the lateral surface of the arch, for protection.
(7) The pharynxes of chimaeroids and hagfish are specialized, whereas those of
heterostracans, osteostracans, and thelodonts were similar to the ancestral
vertebrate pharynx. These ostracoderms did not have a pumping velum.
(8)In the protochordate amphioxus, branchial structures occur only in the pharynx.
This implies that early vertebrates never had premandibular branchial arches or
pouches and that the maxillary nerve (V,) is not a premandibular branchial
nerve.
(9)The lips and premandibular oral structures of larval lampreys, sharks, and
chimaeroids are comparable down to the details of their skeleton, muscles, and
nerves (see Table 1). These animals share homologous upper lips, cheeks, oral
cartilages, oral sphincters, and buccal constrictors. Whereas larval lampreys use
their upper lips and cheeks for burrowing and to define a velum-housing oral
cavity, sharks and chimaeroids use these structures to round the mouth opening
during suction feeding.
(10)A reconstruction of the oro-labial features of the common ancestor of living
agnathans and Chondrichthyes (Fig. 26) suggests that thisjawless animal was a
benthonektonic predator that fed on worms and other slow invertebrates on the
ocean floor, as suggested by Northcutt 8z Gans (1983). The premandibular
ORIGIN OF JAWS
397
mouth and lips of this ancestor, not its mandibular arch, served for prey
capture.
(1 1) The ventilatory origin of gnathostomes is modelled as follows (see Fig. 30):
(a)The common ancestor of all living vertebrates had a predatory lifestyle that
became increasingly more active.
@) With the concomitant selection for stronger ventilation, the branchial arches
and muscles of pre-gnathostomes became more elaborate, strengthening both
expiratory and inspiratory pumps.
(c)The strongest ventilatory muscles were those that shut the mouth during
strong expiration (adductor mandibulae) and rapidly opened the mouth
during forceful inspiration (spinal hypobranchial muscles). Shutting the
mouth prevented anterior reflux of expiratory water from the pharynx. To
accommodate the strong pull of its muscles, the mandibular arch became
larger than any other branchial arch - a set of ventilatory ‘jaws’.
(d) Strong suction and a mouth-closing bite, although evolved for ventilatory
reasons, preadapted the first gnathostomes for sucking in and grasping prey.
When the jaws became feeding structures, they enlarged further, and some
gnathostomes began to take large, evasive, pelagic prey.
(e) In the earliest gnathostomes, the grasping jaws tilted and grew forward, to
encounter prey at the extreme front of the head. This narrowed the oral
cavity anterior to the jaws (old mouth) into a slit, and produced a new mouth
from the anterior pharynx directly behind the jaws.
(12) The new and old mouths are explained in Figures 1C and 3 1B.
(1 3) The aphetohyoid theory, previously discredited because it was wrongly applied
to placoderms and acanthodians, is revived here for ancestral gnathostomes. It
is supported by modern developmental data and by most major groups of
ostracoderms, which had a complete mandibulohyoid gdl pouch.
(14)Two facts argue for a ventilatory, rather than a feeding, origin ofjaws: (i) suction
feeding in jawed fish is an exaggerated ventilatory cycle; (ii) the original feeding
region (the premandibular oral cavity) diminished during the evolution of
gnathostomes, whereas ventilatory structures (the mandibular arch and a new
pharyngeal mouth) increased in size and importance. Gnathostomes feed with
their ventilatory pharynx.
ACKNOWLEDGEMENTS
Thanks are extended to Barbara Stahl, Philippe Janvier, Dominique Didier,
Nicholas Holland, Bernd Fritzsch, Richard Jefferies, Susan Turner, and Peter Forey
for critically reading the manuscript, and especially to Ken Kardong for his interest
in the project and many hours of fruitful discussion.Jeff Christianson at the Seattle
Aquarium helped me to observe feeding radish, and Kevin Swage1 of the Field
Museum of Natural History kindly provided access to preserved chondrichthyans.
NOTE ADDED IN PROOF
After this paper was written, an article appeared reporting chondrichthyan and
thelodont scales from the Middle Ordovician, about 455 million years ago (Sansom,
J. MALLATT
398
I.J., Smith, M. M., Smith, M. P. 1996. Scales of thelodont and shark-like fishes from
the Ordovician of Colorado. Nuture 379: 628-630.) Although, without whole-body
fossils, it is not certain that such ancient chondrichthyans had yet evolved jaws, the
finding still makes chondrichthyans the earliest known gnathostome (or pregnathostome) line; it also means that the great radiation of jawless and pregnathostome fishes that I pictured in Figure 1A at 450 million years ago actually
occurred earlier, before 455 million years ago. The discovery that the oldest known
thelodonts and chondrichthyans were contemporaries indicates that gnathostomes
could not have evolved from any known thelodont, although the two groups could
s till be closely related, as claimed in the present paper.
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