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Origin and Evolution of Gnathostome

Dentitions: A Question of Teeth and Pharyngeal
Denticles in Placoderms

Article in Biological Reviews · June 2005

DOI: 10.1017/S1464793104006682 · Source: PubMed

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Biol. Rev. (2005), 80, pp. 1–43. f Cambridge Philosophical Society 1
DOI : 10.1017/S1464793104006682 Printed in the United Kingdom

Origin and evolution of gnathostome

dentitions: a question of teeth and pharyngeal
denticles in placoderms
Zerina Johanson1 and Moya M. Smith2
1
Palaeontology, Australian Museum, 6 College Street, Sydney, NSW 2010, Australia (E-mail : zerinaj@austmus.gov.au.
ph : 61(2) 9320-6142 ; fax : 61(2) 9320-6050)
2
Craniofacial Development, Dental Institute, Kings College London, and Earth Sciences, University of Bristol
E-mail : moya.smith@kcl.ac.uk: current address: MRC Centre for Developmental Neurobiology, Kings College London
SE1 1UL, UK

(Received 31 March 2004 ; revised 11 November 2004; accepted 16 November 2004 )

ABSTRACT

The fossil group Placodermi is the most phylogenetically basal of the clade of jawed vertebrates but lacks a
marginal dentition comparable to that of the dentate Chondrichthyes, Acanthodii and Osteichthyes (crown-
group Gnathostomata). The teeth of crown-group gnathostomes are part of an ordered dentition replaced from,
and patterned by, a dental lamina, exemplified by the elasmobranch model. A dentition recognised by these
criteria has been previously judged absent in placoderms, based on structural evidence such as absence of tooth
whorls and typical vertebrate dentine.
However, evidence for regulated tooth addition in a precise spatiotemporal order can be observed in placo-
derms, but significantly, only within the group Arthrodira. In these fossils, as in other jawed vertebrates with
statodont, non-replacing dentitions, new teeth are added at the ends of rows below the bite, but in line with biting
edges of the dentition. The pattern is different on each gnathal bone and probably arises from single odontogenic
primordia on each, but tooth rows are arranged in a distinctive placoderm pattern. New teeth are made of regular
dentine comparable to that of crown-gnathostomes, formed from a pulp cavity. This differs from semidentine
previously described for placoderm gnathalia, a type present in the external dermal tubercles.
The Arthrodira is a derived taxon within the Placodermi, hence origin of teeth in placoderms occurs late in the
phylogeny and teeth are convergently derived, relative to those of other jawed vertebrates. More basal placoderm
taxa adopted other strategies for providing biting surfaces and these vary substantially, but include addition of
denticles to the growing gnathal plates, at the margins of pre-existing denticle patches. These alternative strategies
and apparent absence of regular dentine have led to previous interpretations that teeth were entirely absent from
the placoderm dentition. A consensus view emerged that a dentition, as developed within a dental lamina, is a
synapomorphy characterising the clade of crown-group gnathostomes.
Recent comparisons between sets of denticle whorls in the pharyngeal region of the jawless fish Loganellia scotica
(Thelodonti) and those in sharks suggest homology of these denticle sets on gill arches. Although the placoderm
pharyngeal region appears to lack denticles (placoderm gill arches are poorly known), the posterior wall of the
pharyngeal cavity, formed by a bony flange termed the postbranchial lamina, is covered in rows of patterned
denticle arrays. These arrays differ significantly, both in morphology and arrangement, from those of the den-
ticles located externally on the head and trunkshield plates. Denticles in these arrays are homologous to denticles
associated with the gill arches in other crown-gnathostomes, with pattern similarities for order and position of
pharyngeal denticles. From their location in the pharynx these are inferred to be under the influence of a cell
lineage from endoderm, rather than ectoderm. Tooth sets and tooth whorls in crown-group gnathostomes are
suggested to derive from the pharyngeal denticle whorls, at least in sharks, with the patterning mechanisms
co-opted to the oral cavity. A comparable co-option is suggested for the Placodermi.

Key words : Gnathostomata, jawed vertebrates, crown-group gnathostomes, total-group gnathostomes,

Placodermi, dentition, endoderm.
2 Zerina Johanson and Moya M. Smith

CONTENTS

I. Introduction ................................................................................................................................................. 000

II. Gnathostome dentitions and vertebrate phylogeny ................................................................................ 000
(1) Alternative theories on the origin of teeth in stem-group gnathostomes ...................................... 000
(2) Characters of the dentition in crown-group gnathostomes ............................................................. 000
(3) Tooth addition with replacement in jawed vertebrates ................................................................... 000
(4) Phylogenetic relationships of the Placodermi .................................................................................... 000
III. Placoderm dentitions : contribution of teeth and denticles .................................................................... 000
(1) Oral cavity : presence of teeth and denticles ..................................................................................... 000
(a) Arthrodira : arrangement of teeth ................................................................................................. 000
(i) Evidence in coccosteomorph arthrodires for the presence of teeth .................................. 000
(ii) Diversity and arrangement of structures in the coccosteomorph dentition .................... 000
(iii) Juvenile dentitions : toothed rows ......................................................................................... 000
(iv) Evidence in pachyosteomorph arthrodires for the presence of teeth ............................... 000
(b) Other arthrodires : tooth rows and denticulated ‘ areas ’ ........................................................... 000
(i) ‘ Primitive brachythoracids ’ : teeth and denticles ................................................................ 000
(ii) Phlyctaeniida : denticle fields .................................................................................................. 000
(iii) Actinolepida: tooth addition .................................................................................................. 000
(c) Phyllolepida : denticle fields ............................................................................................................ 000
(d) Acanthothoraci : supragnathal plates ............................................................................................ 000
(e) Antiarchi and Rhenanida : external dermal elements in the dentition .................................... 000
(f) Other denticles in the oral cavity: parasphenoid and paraotic plates ...................................... 000
(2) Pharyngeal cavity : presence of pharyngeal denticles ....................................................................... 000
(a) Gill arches and skeletal components ............................................................................................. 000
(b) Postbranchial lamina and denticle pattern .................................................................................. 000
IV. A developmental model from phylogenetic pattern ............................................................................... 000
(1) Ectodermal against endodermal patterning ...................................................................................... 000
(2) Tooth retention and tooth addition ................................................................................................... 000
(3) Tissue growth in teeth and denticles .................................................................................................. 000
(4) Adaptive growth and tissue remodelling ............................................................................................ 000
(5) The placoderm oral cavity ................................................................................................................... 000
(6) The placoderm pharyngeal cavity ...................................................................................................... 000
V. Conclusions .................................................................................................................................................. 000
VI. Acknowledgements ...................................................................................................................................... 000
VII. References .................................................................................................................................................... 000

I. INTRODUCTION there is active disagreement and debate as to the validity of

Classic theories of dental evolution are based on the acqui-
sition of teeth at the jaw margins by the assumed evol-
utionary migration of external skin denticles surrounding
the mouth into the oral cavity (see Jollie, 1968). A develop-
mental mechanism was provided to explain this evolution-
ary pattern of change, from jawless to jawed fishes, in
location of the denticles from skin to oro-pharynx and then
to an enlarged, specialised set at the jaw margins (Reif,
1982). It was assumed that all denticles are homologous
(those of the skin and oro-pharynx, as odontodes, Ørvig,
1977) and that the agreed phylogenetic order of their ap-
pearance was skin denticles first, then oral denticles prior to
teeth at the jaw margins, and lastly, pharyngeal denticles
(Jollie, 1968). However, new fossil evidence on denticle dis-
tribution relative to the origin of jaws has provided an
alternative to this classic consensus view (van der Brugghen
& Janvier, 1993; Donoghue & Smith, 2001 ; Purnell, 2001;
Smith & Coates, 2001). Opinion is currently divided and
these two theories (Smith and Johanson, 2003 a, b ; Burrow,
2003; Miller, Cloutier & Turner, 2003; Young, 2003). Sire
(2001) and Sire & Huysseune (2003) have also advocated a
different definition of teeth, denticles and odontodes as
dermal skeletal elements from studies of development in
extant osteichthyans, including ‘ extra oral teeth ’ (Sire,
2001).
The main objective of this review is to present new data
on the phylogenetic origins of teeth and pharyngeal den-
ticles, focusing on the jawed vertebrate group Placodermi,
phylogenetically basal jawed vertebrates and sister-taxon to
the crown-group Gnathostomata (Fig. 1). We attempt to
establish the phylogenetic sequence in which characters of
the dentition are expressed within the Placodermi including
pharyngeal denticle patterns comparable to those observed
in the thelodont Loganellia scotica Traquair, 1898 (Johanson &
Smith, 2003). We interpret our morphological observations
in the context of a developmental model based on pattern-
ing of tooth addition as identified in extant jawed vertebrates
Origin and evolution of gnathostome dentitions 3

Vertebrata ARTHRODIRA
Brachythoraci
Total Gnathostomata
Eubrachythoraci
Jawed Vertebrates 'primitive
brachythoracids'

coccosteomorphs
Acanthothoraci

Petalichthyida
Ptyctodontida

Phlyctaeniida
Crown Gnathostomata Stem Gnathostomata

Actinolepida

Buchanosteus
Antineosteus
Rhenanida
Antiarchi

Holonema

Maideria
Osteichthyes

Pachyosteomorpha

CEPHALOCHORDATA
CHONDRICHTHYES

PLACODERMI
ACTINOPTERYGII
SARCOPTERYGII

HETEROSTRACI
OSTEOSTRACI

CONODONTA
THELODONTI
ACANTHODII

LAMPREYS
ANASPIDA

HAGFISH
Fig. 2. Cladogram showing relationships of taxa assigned to
the Placodermi (adapted from Goujet & Young, 1995 and
Goujet, 2001) and relationships within the Arthrodira (see also
Fig. 4). Note that in Goujet, 2001, the Rhenanida and
?5 ?5 Acanthothoraci are resolved as sister taxa.
5 5
?5
2, 6 2, 6
2, 4, 6 (1) Do oral denticles derive from denticles on the external
dermal armour, and do these subsequently evolve, with co-
option of their ectodermally derived pattern, into teeth at
the jaw margins? Or (2), does this pattern derive exclusively
3 from that of internal pharyngeal denticles, as such being
1 endodermally derived ? (3) Are pharyngeal denticles them-
selves derived from the posterior migration of skin denticles
into the caudal end of this region, or do they have a distinct
and separate evolutionary history ? Or (4), alternatively, are
they derived from dermal denticles formed at the junctions
Fig. 1. Cladogram showing relationships of jawed vertebrates, of ectoderm with endoderm in the post-cranial region,
including the Placodermi and crown-group Gnathostomata either laterally at each pharyngeal pouch, or solely at the
(adapted from Donoghue et al., 2000, Purnell, 2001). Character sites of the postbranchial laminae ?
states : 1, mineralised skeleton, odontode histogenesis ; 2,
internal mineralised skeleton ; 3, external mineralised skeleton ;
4, jaws ; 5, teeth ; 6, genes responsible for organising and II. GNATHOSTOME DENTITIONS AND
patterning internal skeleton.
VERTEBRATE PHYLOGENY

(1 ) Alternative theories on the origin of teeth in

stem-group gnathostomes
(Smith, 2003), using these data in the placoderm dentition to Classic ideas on the evolutionary origins of teeth suggest that
consider homology with teeth of crown-group gnatho- the denticles became enlarged to form teeth subsequent to
stomes. their migration from external skin to oral margins, as the
Our observations are placed in a phylogenetic context, ectoderm invaginated to form the stomatodeum during
based on recent work by Goujet & Young (1995) and Goujet development of the mouth (Fig. 3; Jollie, 1968). Develop-
(2001 ; Fig. 2) for higher-level placoderm phylogeny and mental mechanisms proposed for this are that teeth devel-
Carr (1995) and Lelièvre (1995) for arthrodiran relationships oped from an innovative tooth-making structure, an
(Figs. 2, 4). Our central objective is to establish in which ectodermally derived tissue known as the epithelial dental
placoderm taxa teeth are present and to determine whether lamina, such that teeth formed out of the bite and deep to
they are restricted to derived taxa within the group, as re- the surface (Reif, 1982; Smith & Hall, 1993, see their Fig. 2).
cently proposed (Smith & Johanson, 2003 b). This tissue structure alone patterned the entire dentition,
Using information from the Placodermi, we attempt to while denticles found posteriorly in the pharyngeal region
address some fundamental questions concerning the evol- originated later in the evolutionary process (Broili, 1933;
utionary origins of jawed vertebrate dentitions. Watson, 1937 ; Halstead Tarlo & Halstead Tarlo, 1965;
4 Zerina Johanson and Moya M. Smith

stom. or.t
ma.a
stom. ph.d

hy.a
phar. phar.
1st. a
ph.d
2nd.a

Wuttagoonaspis
Brindabellaspis
Acanthothoraci

Yunnanolepids
A B

Petalichthyida

Phlyctaeniida

Brachythoraci
Ptyctodontida

Actinolepida

Phyllolepida
Euantiarchi
Rhenanida
sp

C D
pter PBL
phar.
ce.h sp.sk
t.pl hy.h
ba.h
E
Fig. 3. (A–E) Diagrams to show generalised agnathan (A, B)
and gnathostome (C, D) in longitudinal horizontal section, of Antiarchi
Arthrodira
types with both an armoured dermal skeleton (A, D) and one
with separate denticles (placoid scales, B, C). (E) A transverse
section through the pterygoid and hyoid arch in a gnathostome
with denticulated pharyngeal plates (modified from Figs. 3, 4, 5
in Jollie, 1968). These show the limits of the ectoderm (hatched)
and endoderm (shaded), as predicted by Jollie (1968). Double
arrows mark the equivalent position of the postbranchial
lamina (PBL) in placoderms. Establishing the positions of the
ectoderm-endoderm boundary is proposed as a key to pattern
information in development of oro-pharyngeal denticles and
Fig. 4. Cladogram showing relationships within the
oral teeth (or.t). (B) Adapted from Jollie (1968) to show the
Arthrodira. Adapted from Lelièvre (1995) and Carr (1995).
position of pharyngeal denticles (ph.d) based on new infor-
mation in Loganellia scotica. Other abbreviations : 1st.a, 2nd.a,
first and second gill arches ; ba.h, basihyal ; ce.h, ceratohyal ;
hy.a, hyoid arch ; hy.h, hypohyal ; ma.a, mandibular arch ; ventillatory theory, in which jaws evolved first for suction
phar., pharyngeal cavity ; pter, pterygoid ; sp, spiracle ; sp.sk, feeding, while teeth developed at a later stage of gnatho-
splanchno-skeleton ; stom., stomodeum ; t.pl, tooth plates. stome evolution. Also, both systems, jaws and teeth, were
proposed to be independent units in their development, and
thus also change independently during evolution (Smith &
Hall, 1993). Subsequently, it was recognised that although
Jollie, 1968 ; Schaeffer, 1975 ; Burrow, 2003 ; Young, 2003). odontodes shared a homologous developmental programme
As such, these theories assume that mechanisms for the de- for histogenesis, internal oro-pharyngeal denticles and ex-
velopment and pattern regulation of skin denticles became ternal skin denticles possessed different and divergent evol-
co-opted to make teeth, involving an inductive ectodermal utionary histories (Smith & Coates, 1998). Because these
epithelium. Tooth-making ability has been linked to the originate at a phylogenetically basal node in vertebrate
acquisition of jaws, when the mandibular arch moved cau- phylogeny (Fig. 1), one could not be derived from the other.
dally together with the invagination of the ectoderm (Fig. 3; One topographic basis for the difference between oro-
see Fig. 4 in Jollie, 1968). It was assumed that the inner pharyngeal denticles and dermal skin denticles is the pro-
denticulate surface of the first branchial arch was then used posed phylogenetic independence of the visceral skeleton
for food processing at an early phylogenetic stage, with these (splanchnocranium, Kardong, 2002) from the dermal and
changes linked to increasing predatory activity (Jollie, 1968). endoskeletal systems (Donoghue & Sansom, 2002).
In recent years, several aspects of the classic theories Donoghue and Sansom (2002) suggest that this distinction
(Jollie, 1968; Reif, 1982) have been challenged. For ex- occurred at a level below the origin of the Vertebrata (a
ample, rather than accepting an evolutionary link between clade including the last common ancestor of hagfish, lam-
the development of a dentition and articulated jaws during preys, crown-group gnathostomes and all descendants of
increasingly active predation, Mallatt (1998) proposed the this ancestor, including fossil jawless fishes as well as the
Origin and evolution of gnathostome dentitions
Placodermi ; Fig. 1). Oro-pharyngeal denticles and teeth are
included as part of the splanchnocranium, some fused to
splanchnic bones of the palate and dermal bones of the jaws,
along with the supporting branchial cartilages and their
perichondral and endochondral bones (Nelson, 1969,
1970 a ; Donoghue & Sansom, 2002; Kardong, 2002;
Smith, 2003). As discussed below (Section IV.1), splanchnic
structures are hypothesised to be dependent on endoderm,
rather than ectoderm, for pattern information.
Another observation supporting the divergent evolution-
ary histories of internal and external skeletal systems is that
the Conodonta (total-group Gnathostomata, Fig. 1) are the
first vertebrate group to show skeletal mineralisation.
Importantly, this occurs exclusively within the oro-pharyn-
geal cavity, possibly associated with the splanchnoskeleton
(Smith & Coates, 1998, 2000, 2001; Donoghue, Forey &
Aldridge, 2000 ; Donoghue & Aldridge, 2001 ; Donoghue &
Sansom, 2002). Conodont elements show both bilateral
symmetry and antero-posterior differences as evidence of
organisation or patterning. Given their known position in
the conodont animal, ventral and posterior to the eyes, they
are topographically co-incident with other feeding struc-
tures ; the anterior elements could be part of the oral cavity,
with the more posterior part of the pharyngeal apparatus
(Donoghue & Purnell, 1999, see their Fig. 1). Other early
total-group gnathostomes (Heterostraci, Anaspida,
Osteostraci, Fig. 1) are characterised by a heavily min-
eralised dermal armour and the apparent absence of
internal dermal structures (Smith & Coates, 1998, 2000,
2001 ; Donoghue & Sansom, 2002). Although Donoghue &
Sansom (2002) suggest that these internal and external el-
ements can shift topographically between these regions, in-
cluding from internal to external, in fact the two regions are
distinct at the early phylogenetic stage represented by the
Conodonta.
As a new theory distinct from the classic one, Smith &
Coates (1998, 2000, 2001) suggested that the essential pat-
terning mechanisms required for the tooth sets characteristic
of crown-group Gnathostomata evolved from the co-option
of regulatory mechanisms associated with organised internal
pharyngeal denticles in the jawless vertebrate Loganellia sco-
tica Thelodonti ; Section IV.1). Significantly, as with the
Conodonta, this was prior to the appearance of jaws. This
new hypothesis essentially reversed the inferred polarity of
dental evolution. Rather than an external origin from der-
mal denticles with embryonic ectoderm recruited to make
teeth at the mouth margins, an internal origin from embry-
onic endoderm of the pharyngeal cavity was proposed. For
example, the initial iterative pattern in the zebrafish Danio
rerio pharyngeal region is dependent on endodermal signal-
ling, which is also required to make the separate cartilages in
the branchial arches (Piotrowski & Nüsslein-Volhard, 2000).
Donoghue (2002) noted that the external skeleton (scales) is
patterned, in a manner comparable to other dermally de-
rived elements such as feathers, however, this patterning
involving the ectoderm differs significantly from patterning
associated with the splanchnocranium and with structures
such as the denticle/tooth whorls.
Despite these attempts to revise the theories on the
origin of teeth, their origin from developmentally distinct
5
pharyngeal denticles has been questioned in recent pub-
lications. The first, by Purnell (2001), demonstrated that
amongst other jawless vertebrates (Heterostraci, Fig. 1), oral
denticles at the mouth margin of heterostracans intergraded
morphologically with dentine ridges on the external head-
shield. Thus, Purnell (2001) concluded that external dermal
structures gave rise to oral denticles in heterostracans, as
predicted by the more traditional theories of dental evol-
ution. The heterostracan oral denticles also show a degree of
organisation, such that the denticle tips are oriented out-
wards, leading Purnell (2001) to suggest that the develop-
mental differences between oro-pharyngeal denticles and
skin denticles in thelodonts described by Smith & Coates
(1998) were not significant. However, both thelodonts and
elasmobranchs have comparably oriented denticles in the
prenasal sinus and inhalent nasal openings, both respect-
ively, derived from ectoderm (van der Brugghen & Janvier,
1993 ; Purnell, 2001). Denticles associated with the bran-
chial arches in the pharyngeal region of Loganellia scotica are
significantly different from the more anterior oro-nasal
examples (Smith & Coates, 2001), forming joined sets or
whorls with sequential addition from one direction only.
Regulation of the pharyngeal system would appear to be
more comparable to the patterned tooth sets in crown-group
gnathostomes than either those of skin, oral or nasal den-
ticles, and hence more likely to have been co-opted as a
developmental system to pattern dentitions.
Miller et al. (2003, Section II.4) have recently described
the earliest known articulated shark in which they noted that
the branchial denticles differed morphologically from teeth
in the jaw. Tooth families were visible and showed newer
teeth sitting in a space representing the dental lamina. We
can conclude from Miller et al. (2003) that the tooth system
was well regulated from a dental lamina and that this con-
tinued along the length of the jaw to the more posterior
tooth families, which are also distinctly different from the
pharyngeal denticles. However, Miller et al. (2003) state that
these posterior tooth sets are more similar to modified der-
mal scales, based on absence of ‘the dental membrane ’.
They suggested this evidence, and the differences between
pharyngeal denticles and teeth, contradicted an origin of
teeth from pharyngeal denticles. However, the term ‘ dental
membrane ’ is obscure and not properly defined by the
authors and we suggest that these posterior sets are teeth,
developing from a superficial dental lamina, rather than
scales. Differences between teeth and branchial denticles
are misunderstood by the authors, as the concept advanced
by Smith & Coates (1998, 2000, 2001) suggests that it
is the regulatory and patterning mechanisms for sets of
denticles that are co-opted, not just denticle morphology.
Furthermore, denticles in the anterior mucous membranes
near the mouth margin are polygonal in shape, differing
morphologically from the rounded external skin denticles of
the head, suggesting a separation, rather than continuation
of, or gradation between, these denticulated areas. Contrary
to the authors’ views, this does not support classic theories of
dental evolution.
In a phylogenetically based critique, Donoghue & Smith
(2001), using new analyses, argued that Loganellia scotica is
derived within the Thelodonti, rather than resolved to a
6 Zerina Johanson and Moya M. Smith
position at the base of the group. Branchial whorls are not
known from the more basal thelodonts and based on this
phylogenetic resolution the derivation of tooth whorls from
denticle whorls in Loganellia scotica is problematic. Similarities
in organisation within the denticle whorls (Loganellia scotica)
and tooth whorls (crown-group gnathostomes) observed by
Smith & Coates (1998, 2000, 2001) would be convergently
acquired.
Burrow (2003), commenting on Smith & Johanson’s
(2003 b) identification of teeth in derived placoderm groups,
suggested that more basal placoderm groups possessed not
teeth, but tubercles, on the dental plates, organised in the
same manner as the ‘teeth ’ identified by Smith & Johanson
(2003 b). Burrow (2003) suggested that the tubercles on the
dental plates are not randomly distributed in these basal
placoderm groups, such as the Acanthothoraci, Rhenanida
and Antiarchi (Figs. 2, 4), a contention discussed, and re-
futed in Section III.1d–f. Burrow (2003, see her Fig. 1 A)
identified a gnathal plate from the Acanthothoraci and
suggested that the arrangement of tubercles on this plate was
comparable to external skin tubercles on the head and
trunkshield plates. This led her to conclude that oral den-
titions were derived from external skin tubercles, as suggested
by classic theories of dental evolution. However, as noted by
Smith & Johanson (2003a), the particular microvertebrate
specimens Burrow (2003) illustrates as being an acantho-
thoracid placoderm are of uncertain affinity, in all prob-
ability acanthodian.
Young (2003) also supported the derivation of all placo-
derm dentitions from external skin tubercles and queried the
characters specified by Smith & Johanson (2003 b) to identify
teeth in placoderms. He noted, as we have, that external
dermal tubercles are also patterned (as discussed above,
Donoghue, 2002), justifying this by illustrating a row of
pointed tubercles along the edges of the arthrodiran spinal
plate and antiarch pectoral fin. However, Young’s (2003)
suggestion that these denticles satisfy the criteria used for the
recognition of teeth by Smith & Johanson (2003b), is not
adequately supported by his own figures (Fig. 1E–G in
Young, 2003, also Stensiö, 1948). We maintain that teeth
(Young’s ‘ denticles ’) in brachythoracid arthrodires differ
from external tubercles in their spatiotemporal regulation
and see no evidence to refute this (Smith & Johanson,
2003a, b). Differences between oral denticles on the phlyc-
taeniid Dicksonosteus arcticus Goujet, 1975 (Fig. 10 H) and
tubercles on the external surface of headshield plates are
readily apparent (see plate 5, 2b, 5a, in Goujet, 1975;
Figs. 39, 41, 42, and plate 8.5B, 8.6A in Goujet, 1984 a).
External dermal elements are incorporated into the den-
tition of two phylogenetically basal placoderm groups
(Section III.1e), but these are not teeth, nor do they form
part of a patterned dentition, nor are the dentitions of more
advanced placoderms derived from these.
(2 ) Characters of the dentition in crown-group
gnathostomes
Although teeth and skin denticles or tubercles are hom-
ologous at the tissue development level (Ørvig, 1977;
Schaeffer, 1977; Smith & Hall, 1990 ; Donoghue, 2002), the
mechanisms regulating their respective developmental pat-
terning (Donoghue, 2002) and specifying the positions for
addition and replacement of teeth are non-homologous. As
noted above, their divergent evolutionary histories (Smith
& Coates, 1998, 2001 ; Smith, 2003) (Section II.1) can be
traced to the base of the total group Gnathostomata and the
Conodonta (Fig. 1).
In the oral cavity both teeth and oral denticles are used to
build dentitions in crown-group gnathostome taxa but the
use of these terms as defined by Ørvig (1977) and Reif (1982)
is often not stringently applied (Smith, 1988). Distinction
between the two terms involves developmental concepts and
may be difficult to apply to fossil taxa (Schaeffer, 1977 ; Reif,
1982). This can cause confusion and lack of precision in
comparisons between dentitions (for a discussion on lungfish
dentitions see Smith, 1988). Distinctively new teeth form
within a dental lamina below the biting surface of the jaw
and in advance of participation in the bite. By contrast,
denticles develop superficially, are widely dispersed, and
form when a space becomes available due to general or local
growth, or loss of a previous denticle. From these topo-
graphical criteria, both the arrangement and relative timing
of addition can be deduced.
In particular, the position of putative tooth primordia can
be inferred from the presence of a regulated and organised
sequence of tooth addition, exemplified by tooth whorls in
fossil taxa, but said to be absent in placoderms (Reif, 1982).
In extant chondrichthyans (sharks, rays, and holocephalans),
tooth ‘families ’ or ‘sets ’ have been recognised, with the
position of the tooth primordia in a deep epithelial fold
(dental lamina). The newest teeth added to sets in early
growth stages are the largest and the locations of tooth pri-
mordia are not random, but part of an organised, timed
sequence, regulated proximo-distally at the initiation stage
of the dentition (Reif, 1976, 1984 ; Smith & Coates, 2001).
Theoretical models for patterning tooth development and
replacement in crown-gnathostome dentitions have recently
been reviewed (Smith, 2003). Several taxa possess a stato-
dont dentition, where teeth are not replaced but are retained
in the tooth set (Jaekel, 1901 ; Patterson, 1992) and joined at
their bases, with the newest teeth showing lyodont addition
(from the lingual side of the jaw). These terms have been
discussed for holocephalans (Patterson, 1992), other chondri-
chthyans (Smith & Coates, 1998), acanthodians and placo-
derms (Ørvig, 1973), and in general by Smith & Coates
(1998, 2000, 2001) where the condition is considered to be
primitive for jawed vertebrates. In many osteichthyians
(bony fish), teeth are individually replaced except for tooth
whorls at the jaw symphysis, but there are also taxa with
a completely statodont dentition, notably the dipnoans
(Denison, 1974; Smith, 1988). Tooth whorls have been
noted in sarcopterygians [Psarolepis romeri Yu, 1998 (Zhu, Yu
& Janvier, 1999), porolepiforms (Jarvik, 1972), onychodonts
(Jessen, 1966; Long, 2001)] and a very limited number of
actinopterygians (e.g. Howqualepis rostridens Long, 1988). In
the fossil group Acanthodii, these tooth whorls occur not
only at the jaw symphysis, but also as individual whorls, or
sets, along the jaw margin in certain taxa [Brochoadmones
milesi Bernacsek & Dineley, 1977 (Gagnier & Wilson, 1996)].
Other acanthodians (Family Ischnacanthidae ; Long,
Origin and evolution of gnathostome dentitions
1986) possess rows of evenly spaced teeth of graded size, in
which the largest represents the newly added tooth (Smith,
2003).
The statodont condition is also recognisable in placoderm
dentitions, with the cutting edges and tusks of the gnathalia
maintained as continuous growth regions. In statodont
dentitions teeth are added at the growth margins but the
older teeth are not shed as they are worn down and incor-
porated at the cutting edges, so that strictly in situ replace-
ment does not occur. The contribution of teeth to these
surfaces was proposed by Ørvig (1980 a), and recently re-
evaluated by Smith & Johanson (2003b), most notably
within the Arthrodira. In this taxon examples of new teeth
and older teeth, as part of the regulated tooth-addition unit,
can all be observed in a variety of well-preserved taxa (see
Section III.1a, b).
(3 ) Tooth addition with replacement in jawed
vertebrates
Tooth replacement patterns in fish, amphibians and reptiles
have been reviewed by Berkovitz (2000) and the develop-
mental models for these by Smith & Coates (2001) and
Smith (2003). The developmental mechanisms of this re-
placement relative to the dental lamina (Reif, 1982), either
continuous or discontinuous, and the regulatory genes con-
trolling the pattern of tooth positioning are now being
studied in fish (Fraser, Graham & Smith, 2004 ; Laurenti
et al., 2004). Laurenti et al. (2004), reporting on the zebrafish
pharyngeal teeth, implicate one gene in particular (Eve1)
with epithelial initiation of the first tooth primordium in
each dentate region. Fraser et al. (2004) report on epithelially
expressed genes (Shh, Pitx2) important in creating both first
and replacement teeth in the trout Oncorhyncus mykiss and
show that the same genes are deployed in trout, in oral and
pharyngeal teeth, at exactly equivalent stages of tooth de-
velopment as in the mouse. They conclude that the genes
needed to build a dentition are conserved from fish to
mouse, thus a molecular tool kit for making teeth emerged
early in vertebrate evolution.
Amongst pharyngognath fish (functional teeth only found
on the pharyngeal arches), the cichlids (Teleostei : Cichlidae)
are noted for their phenotypic plasticity, forming in
Astatoreochromis alluaudi fine sharp teeth or large molariform
teeth in response to changes in diet as the teeth are cyclically
replaced (Greenwood, 1965 ; Huysseune, 1995, 2000). Initial
teeth form directly from the pharyngeal epithelium but
tooth replacement is from the dental lamina deep in the
bone, whereas other replacement pharyngeal teeth form
from the dental epithelium of the predecessor tooth
(Huysseune, Sire & Meunier, 1994 ; Huysseune, 1995;
Huysseune & Sire, 1998). Most recently, this epithelium is
considered to be a stem cell population (Huysseune &
Thesleff, 2004) where together with odontogenic (tooth-
producing) mesenchyme it can form a tooth primordium for
a replacement tooth. There can be little doubt that in both
the developmental and functional senses, true teeth form in
pharyngognaths despite their location on the fifth branchial
arch. Importantly, they are truly a part of the splanchno-
skeleton and under the putative inductive influence of
7
endoderm lining the pharyngeal cavity (Huysseune et al.,
2002 ; Section IV.1).
Recent comparisons between chondrichthyans and bony
fishes have suggested that the concept of a ‘dental primor-
dium ’, or ‘ tooth clone ’ sensu lato, responsible for forming
new teeth in each set, explains observed morphologies,
particularly in bony fishes (Smith, 2003). In tooth replace-
ment on the jaw of the trout Oncorhynchus mykiss (Berkovitz,
1977) and Polypterus senegalus (Cuvier, 1829) (Clemen,
Bartsch & Wacker, 1998), the new teeth form from the
dental epithelium at the base of the old one (comparable to
the cichlids above). In these examples tooth addition loci are
close to functional teeth rather than deep within a continu-
ous dental lamina along the jaw margin as in elasmobranchs
(Reif, 1982). Positions of the first tooth loci along the
jaw determine where each new replacement tooth-germ
forms. In this way, odontogenic cells (a clonal group, see
Smith, 2003) of the initiator tooth buds form the primary
(original) pattern and autonomously regulate the secondary
replacement pattern. We suggest that these observations on
the variability of development in osteichthyan and chondri-
chthyan dentitions provide criteria for the recognition of
different dentition patterns in fossil forms, for example, re-
lated to identifiable locations of tooth initiation and addition.
In Section III, we apply these criteria to the Placodermi.
(4 ) Phylogenetic relationships of the Placodermi
The Placodermi was first erected by M’Coy (1848) to in-
clude the groups Antiarchi and Arthrodira, but also what we
now recognise as a jawless fish, Psammosteus Agassiz, 1845
(Heterostraci). Traquair (1888) restricted antiarchs and
arthrodires (the genus Coccosteus Agassiz, 1844) to the group
Placodermata Owen, 1860, but later, Cope (1889) assigned
the Antiarchi to the Ostracodermi, along with pteraspid
(Heterostraci) and cephalaspid (Osteostraci) jawless fishes.
The Antiarchi were believed to lack jaws, and Cope’s (1889)
classification persisted for many years (Woodward, 1891;
Dean, 1895; Goodrich, 1909). As well, Woodward (1891;
Dean, 1895) allied the Arthrodira with the Dipnoi (lungfish).
Thus, the Placodermi have not always been considered a
monophyletic group. However, in-depth study of anaspid
and cephalaspid jawless fishes made it clear that these were
very different from the Antiarchi (Kiaer, 1924 ; Stensiö,
1927) and shortly after, upper and lower jaw elements were
discovered for the Antiarchi (Stensiö, 1931). Stensiö (1927,
1931) returned to the usage of the Placodermi including only
the Antiarchi and Arthrodira (or Euarthrodira, at that time
including all other taxa currently assigned to the Placodermi,
also Stensiö, 1969) and suggested they were most closely
related to elasmobranchs (Chondrichthyes).
Placoderm monophyly was also questioned by workers
who noted similarities between the Holocephali (Chondri-
chthyes) and the Arthrodira (Stensiö, 1925, 1934) and
between the chimaeroids (Holocephali) and the placoderm
group Ptyctodontida (Holmgren, 1942). However, some of
these similarities have been shown to be non-homologous
(Patterson, 1965, 1992; Gardiner, 1984 b ; Forey & Gardi-
ner, 1986), and currently the Ptyctodontida are retained
within the Placodermi (Figs. 2, 4).
8 Zerina Johanson and Moya M. Smith
Attempts to evaluate the relationships of taxa assigned to
the Placodermi in a phylogenetic framework have been
made by a variety of researchers (Miles & Young, 1977;
Denison, 1978 b ; Young, 1980 ; Gardiner, 1984b ; Goujet,
1984b ; Forey & Gardiner, 1986 ; Goujet & Young, 1995). In
these analyses, the Arthrodira, in its modern usage (Figs. 2,
4), is resolved as one of the most derived groups within the
Placodermi. Discrepancies amongst the phylogenies have
mainly centred on the positions of the groups Antiarchi and
Ptyctodontida and monophyly of the Acanthothoraci. In
recent analyses, certain poorly understood groups have been
excluded, for example, the Stensiöellida and Pseudopeta-
lichthyida, with some question as to whether these belong to
the Placodermi (Janvier, 1996a). With regards to the Ptycto-
dontida, Miles & Young (1977) retained the group within
the Placodermi, but suggested that their phylogenetically
basal position was based on the presence of the pelvic and
pre-pelvic claspers, otherwise present in chondrichthyans
(holocephalians having both structures, elasmobranchs
having the pelvic claspers alone). Other placoderms were
considered derived in the absence of these claspers (Miles &
Young, 1977). However, the chondrichthyan pelvic and
pre-pelvic claspers are supported by cartilage, but in the
ptyctodont Ctenurella, claspers consist only of dermal spines
or plates, with no cartilaginous support. This led Forey and
Gardiner (1986; also Gardiner, 1984b) to suggest that
ptyctodont and chondricthyan claspers were not homol-
ogous. In Forey and Gardiner’s (1986) analysis, ptyctodonts
are still the most basal placoderm taxon, lacking a pre-
pectoral process on the scapulocoracoid, dorsal narial
openings and sensory canals in open grooves. However, in
other analyses (Goujet, 1984 b), the absence of dorsal narial
openings is shared between arthrodires and ptyctodonts (see
below) and the presence of sensory canals in tubes, rather
than open grooves, is shared with petalichthyids (these are
shown as reversals in Forey & Gardiner, 1986). In current
analyses, the Acanthothoraci is resolved to the basal position
within the Placodermi (Goujet & Young, 1995).
In most phylogenies, the Antiarchi was considered to be
the sister group of the Arthrodira, based on the greater
length of the trunkshield relative to other placoderm taxa,
considered to be the derived condition (Miles & Young,
1977; Denison, 1978b ; Young, 1980; Gardiner, 1984b ;
Forey & Gardiner, 1986 ; Goujet & Young, 1995). By con-
trast, Goujet (1984 b) focused on characters of the head-
shield, including the dorsal position of the nasal openings
and the presence of a premedian plate, which led to a hy-
pothesis of relationships between the Antiarchi, Rhenanida
and Acanthothoraci. In the most recent available clado-
gram, these three groups are resolved to sequential nodes
near the base of the cladogram, again with Arthrodira as
one of the most derived taxa (Figs. 2, 4 ; Goujet & Young,
1995). In previous phylogenies, the Acanthothoraci
(=Palaeacanthaspida) was a monophyletic group, based on
the posterior projection of the paranuchal plates of the
headshield (Miles & Young, 1977; Young, 1980 ; Gardiner,
1984b). However, in the cladogram presented by Goujet
(1984 b), the Acanthothoraci are paraphyletic, with some
taxa more closely related to antiarchs and others to the
Rhenanida. Janvier (1996a) also noted that the group lacked
any synapomorphies. Nevertheless, most recent phylogenies
(Goujet & Young, 1995 ; Goujet, 2001) have retained a
monophyletic Acanthothoraci, suggesting previous analyses
(Goujet, 1984 b) were based on poor data from incomplete
specimens.
Phylogenies addressing relationships of taxa assigned to
the Placodermi have been varied in their resolution of indi-
vidual groups, as has the position of the Placodermi within
the clade of jawed vertebrates. Discussions in the upcoming
sections follow recent phylogenies suggesting that placo-
derms are phylogenetically the most basal group within the
clade (Schaeffer, 1975 ; Schaeffer & Williams, 1977 ; Young,
1986; Coates & Sequeira, 2001 ; Goujet, 2001 ; Janvier,
2001; Zhu & Schultze, 2001). Other researchers have
suggested a closer relationship of the Placodermi to
chondrichthyans within the group Elasmobranchiomorphi
(Stensiö, 1925, 1927, 1931). Still others have proposed
that placoderms and osteichthyans (sarcopterygians+
actinopterygians) are sister taxa, based on putative homol-
ogies between placoderm trunkshield plates and ostei-
chthyan shoulder girdle bones (Jarvik, 1944 ; Stensiö, 1959),
including a denticulated postbranchial lamina, among other
characters (Forey, 1980 ; Gardiner, 1984 b). However, these
homologies have been questioned (e.g. Young, 1986) and
are not supported by recent phylogenetic analyses (Zhu &
Schultze, 2001).
It is important to note that currently the monophyly of the
Placodermi is based on a small number of characters that
have not been tested in a phylogenetic analysis of the entire
clade of jawed vertebrates (Goujet, 1982; Young, 1986 ;
Janvier, 1996 a ; Coates & Sequeira, 2001). Outgroup com-
parison, necessary for determining character polarity, is also
problematic. The recent analysis of Goujet & Young (1995)
used a ‘hypothetical ancestor ’ to code the plesiomorphic
state for all characters, which is not entirely satisfactory.
Other researchers determined the plesiomorphic and de-
rived conditions for various characters by evaluating their
distribution within the Placodermi. For example, with re-
gards to the trunkshield, Miles & Young (1977, p. 131) de-
scribed the plates present in the ‘ primitive placoderm ’ by
noting which plates were found among the widest range of
placoderm groups. When outgroup comparisons are made,
taxa utilised were often other jawed vertebrates (Miles &
Young, 1977; Denison, 1978b, Gardiner, 1984b ; Forey &
Gardiner, 1986).
However, in order to determine character polarity in a
group resolved to the basal node of a major clade like the
jawed vertebrates, it is more appropriate to use the most
closely related taxon outside this group, i.e. a jawless fish
taxon. However, problems arise because these jawless
fishes differ from members of the jawed vertebrate clade in
many respects (Osteostraci) and are often known poorly,
particularly internally (Heterostraci, Anaspida, Thelodonti).
The Osteostraci are currently resolved as the sister group
to the jawed vertebrate clade (Janvier, 1996 b; Donoghue
et al., 2000 ; Donoghue & Smith, 2001). These have been
used as an outgroup to polarise character states within
the jawed vertebrates and less frequently, the Placodermi
(Coates & Sequiera, 2001 ; Janvier, 2001; Johanson, 2002).
For example, the osteostracan Norselaspis possesses a
Origin and evolution of gnathostome dentitions
scapulocoracoid with an articular surface for a single
fin radial and surrounding depressions for fin muscles and
foramina for nerves and blood vessels comparable to the
scapulocoracoid of jawed vertebrates (Janvier, 1985, 1996 a).
Comparisons between the course of these vessels in osteo-
stracans and the Antiarchi suggested that the antiarch
condition is plesiomorphic relative to the rest of the
Placodermi and other jawed vertebrates, such that these
taxa share a derived character that the Antiarchi lack
(Johanson, 2002). This challenges placoderm monophyly
but again has not been tested within a rigorous phylogenetic
analysis.
Placoderm non-monophyly could result in those taxa
(Arthrodira) with teeth being resolved as more closely re-
lated to crown-group gnathostomes than other placoderms.
In this instance, teeth would not be independently derived
within the placoderms, but consideration would still need to
be given to the absence of teeth early in chondrichthyan and
possibly acanthodian history (Turner & Young, 1987; Long,
1995 ; Janvier, 1996a ; Wilson, Hanke & Sahney, 1999;
Williams, 2001). Miller et al. (2003) described the earliest
articulated chondrichthyan currently known, from the early
Devonian (Emsian), a specimen with up to fifteen spaced
and organised sets of teeth at the jaw margin. However,
even earlier articulated shark specimens from the Early
Devonian (Lockhovian) of the Canadian Arctic have been
described as lacking teeth, leading Wilson et al. (1999) to
propose an independent origin of teeth within the chondri-
chthyans. As well, in some of the earliest known chondri-
chthyan faunas from the Silurian of Russia and Asia, dermal
scales are present but teeth are not. This includes taxa which
may represent one of the most plesiomorphic chondri-
chthyan groups, such as those assigned to the Mongolepida
(Karatjute-Talimaa, 1973 ; Karatjute-Talimaa et al., 1990).
Even earlier ‘chondrichthyan-like ’ scales, but not teeth,
have been described from the Ordovician of Colorado
(Sansom, Smith & Smith, 1996).
III. PLACODERM DENTITIONS :
CONTRIBUTION OF TEETH AND DENTICLES
In current phylogenies, the Placodermi are the most plesio-
morphic group to possess jaws and should provide import-
ant data on the distribution of teeth and denticles at this
stage of evolution, relative to jawless vertebrates such as
Loganellia scotica and the Heterostraci and jawed vertebrates
included in the crown-group Gnathostomata. We provide
below new data and reassess published information on the
feeding apparatus in all placoderm groups, together with a
review of denticle distribution in the pharyngeal region
based on Johanson and Smith (2003).
One current opinion is that teeth (those derived from
a dental lamina) are a synapomorphy of crown-group
gnathostomes present in all jawed vertebrates except placo-
derms (Denison, 1978 b ; Reif, 1982 ; Goujet, 2001; Young,
Lelièvre & Goujet, 2001; Zhu & Schultze, 2001 ; Donoghue
& Sansom, 2002 ; Burrow, 2003 ; Young, 2003). Equally,
9
pharyngeal denticles are considered to be absent in placo-
derms (Donoghue & Smith, 2001), although they are present
in basal chondrichthyans and osteichthyans. Pharyngeal el-
ements are largely unknown in acanthodians except for gill
arches and accompanying rakers in Acanthodes bronni Agassiz
1833 (Miles, 1973).
The absence of teeth in placoderms has been justified for
three reasons. First, tooth whorls, or spirals, are absent from
placoderm jaws ; these whorls providing the structural evi-
dence that a tooth-producing dental lamina is present in the
crown-group gnathostomes, including the fossil group
Acanthodii (Reif, 1982). For example, Young et al. (2001;
also Young, 2003) recently emphasised the lack of order, or
patterning (i.e. into whorls or spirals) of the denticles on the
gnathalia of certain arthrodires (the group Phlyctaeniida;
Figs. 2, 4). The second reason is the apparent absence of
regular dentine in the dental tissues ; Young et al. (2001)
emphasised the histological similarity of the denticles to the
dermal tubercles on the external surface of the dermal plates
of the head and trunkshield (see Section III.1.a, b). This
variant of dentine has been described in both the arthrodire
dentition and shield tubercles as semidentine (Ørvig,
1980 a). Linked with this is the absence of a pulp cavity
normally found in teeth, but not in dermal tubercles. Third,
as universally accepted, an enamel covering is absent (Gross,
1957 ; Ørvig, 1973 ; Denison, 1978 b).
Contrary to these views, Smith & Johanson (2003 a, b)
described morphological and histological evidence for the
presence of teeth in Placodermi, in the derived group
Arthrodira, although the phylogeny indicated non-hom-
ology with teeth in other jawed vertebrate clades (Figs. 1, 2).
Because more phylogenetically basal placoderms such as the
Antiarchi and Rhenanida (Figs. 2, 4) lack these tooth rows,
teeth evolved independently within the group. The mor-
phological evidence demonstrated that new teeth, with a
gradual size increase and similar shape polarity, were con-
sistently added to the ends of pre-existing rows, below the
functional bite. Hence, the arthrodiran tooth row is very
similar to a crown-gnathostome tooth whorl or family, and
we have compared it to a statodont tooth row, as in dipno-
ans. However, the more phylogenetically basal placoderms
lacking these criteria cannot be said to possess teeth and
are relevant in discussions of the origins of placoderm
teeth, whether from external skin tubercles, or internal phar-
yngeal denticles, because their edentate condition suggests
arthrodiran teeth are neomorphic.
(1 ) Oral cavity : presence of teeth and denticles
We follow a developmental model of tooth addition to the
dentition (Smith, 2003) and apply this to the Placodermi, to
allow us to identify the evolutionary origins of the tooth-
additive type of dentition and further to assess homologies
with teeth in crown gnathostomes. This model is based on
the statodont dentition, which essentially preserves the en-
tire ontogeny of the dentition (e.g. the lungfish toothplate),
allowing developmental and growth processes to be inferred
and positions of newly added teeth to be identified (see
Ørvig, 1980 a). The functional part of the dentition, worn
teeth, also tusks and cutting edges, forms from non-replaced
10
teeth. The developmental model of tooth addition as pro-
posed is defined as follows :
(1) a tooth regional field (with odontogenic restriction
boundaries) is associated with each dentate (gnathal) bone
(Donoghue, 2002 ; Fraser et al., 2004). Within each field, a
single separate primordium (dental placode, or clonal group
of cells, gene expression centre ; Smith, 2003; Fraser et al.,
2004; Laurenti et al., 2004) initiates the placoderm specific
pattern for sequential tooth addition. Based on new evi-
dence for the sequential, reiterative pattern of tooth
initiation and morphogenesis of mammalian teeth (Jernvall
et al., 2000), each primordium (dental placode) will act as
a tooth signalling centre.
(2) Genetic mechanisms responsible for the tooth re-
gional field in (1) and the pattern of sequential, reiterative
tooth development could be part of a hierarchical develop-
mental module for tooth sets. In the early manifestation of
this, one phylogenetic stage is oral denticles added to the
margins of gnathal plates, but not in regular well-spaced
rows.
(3) New teeth develop in relation to the initial tooth site
and are regulated as proposed in the clonal model for a
discontinuous dental lamina (Reif, 1982 ; Smith, 2003) and
by expression of epithelial genes (Fraser et al., 2004).
(4) Teeth are added to a recognisable, statodont, tooth
row linking the original tooth to later, regularly spaced
functional teeth where each is supported by a new bone of
attachment. Functional, worn teeth and newly added teeth
are often incorporated and transformed into cutting edges
and tusks (Section IV.3, 4) by an adaptive mechanism of
pleromic growth of dentine into the bone (see Smith &
Sansom, 2000).
(5) New teeth of tubular dentine grow from the pulp, as
in the crown-gnathostome-type. Only after further growth
related to wear does this transform into semidentine (Section
IV.4), the type that occurs in the dermal tubercles.
Most aspects of this model can be readily recognised in
the statodont dentition of arthrodiran taxa, and from the
observed pattern of growth the genetic patterning processes
are inferred. Placoderm feeding structures are organised
into a single pair of lower jaw elements (infragnathals) and
upper jaw elements known as anterior and posterior
supragnathals (Fig. 5, IG, ASG, PSG respectively). Each
infragnathal comprises a bony structure supported on
Meckel’s cartilage ; the latter is endochondrally ossified to
varying degrees in different taxa, but the infragnathal is a
membrane bone and, therefore, ossified throughout its ex-
tent (Figs. 6 B, F, G and Figs. 7–9). The anterior and pos-
terior supragnathals (Figs. 6A, C, D and 7 A–G, I–K) are
supported on the endocranium, on the ethmoid and auto-
palatine (as part of the palatoquadrate) respectively.
Homology of the upper feeding structures in the Antiarchi
(Fig. 10 I, J) and the Rhenanida (e.g. Nefudina qalibahensis
Lelièvre et al., 1995) to the supragnathals is problematic
(Section III.1,e).
Based on the current developmental model, the best
evidence for teeth amongst placoderms is provided by
the derived group Arthrodira (Fig. 2; Goujet & Young,
1995; Goujet, 2001). The Arthrodira can be divided into
the Actinolepida, Phlyctaeniida and Brachythoraci (Fig. 4;
Zerina Johanson and Moya M. Smith
ASG
PSG
IG
Fig. 5. Coccosteus cuspidatus Miller, 1841 ex Agassiz ms. Anterior
view of headshield, anterior and posterior supragnathals and
infragnathals (all shaded). Adapted from Miles & Westoll
(1968). Abbreviations : ASG, anterior supragnathal ; IG, infra-
gnathal ; PSG, posterior supragnathal.
Denison, 1978b ; Carr, 1995 ; Goujet, 2001) although only
the Actinolepida and Eubrachythoraci (Fig. 4) possess dental
morphologies most readily compared to the statodont
condition of various chondrichthyans, acanthodians and
osteichthyans. Dentitions of the ‘primitive brachythoracids ’
possess tooth rows in addition to areas or patches of den-
ticles. Among the Arthrodira, only the Phlyctaeniida appear
to lack tooth rows; instead denticles are added to the mar-
gins of the gnathal plates of the dentition, showing some
degree of regulation. A comparable pattern is seen within
the group Phyllolepida.
( a ) Arthrodira : arrangement of teeth
As indicated in Figs. 2 and 4, the Arthrodira includes the
Actinolepida, Phlyctaeniida and the Brachythoraci, the lat-
ter containing two large groups, the coccosteomorphs and
the pachyosteomorphs, along with the ‘primitive brachy-
thoracids ’. Our descriptions start with the most derived
arthrodiran taxa (Figs. 6–9, and 11), and proceed to the base
of the clade, concluding with the Actinolepida (Fig. 10A–D ;
Denison, 1958).
(i ) Evidence in coccosteomorph arthrodires for the presence of
teeth. Coccosteomorph taxa examined for this description
include Kimberleyichthys whybrowi Dennis-Bryan & Miles,
1983, Harrytoombsia elegans Miles & Dennis, 1979, Incisoscutum
ritchiei Dennis & Miles, 1981, Gogopiscis gracilis Gardiner &
Miles, 1994, Compagopiscis croucheri Gardiner & Miles, 1994
and Bullerichthys fascidens Dennis & Miles, 1980 (Fig. 7 I, J ;
also Dennis-Bryan & Miles, 1983 ; Gardiner & Miles, 1990).
The supragnathals of these coccosteomorph taxa possess
rows of teeth, frequently two on the anterior and three on
the posterior (Fig. 7 A–G). These rows meet at (or radiate
from) a single point on the supragnathal, representing both
the growth centre of the gnathal element (gr.c) and the
location of the original tooth primordium. Two or three
Origin and evolution of gnathostome dentitions 11

Fig. 6. (A–F) Dunkleosteus terrelli (Newberry, 1874). (A, C). Right posterior supragnathal, CMNH 5848, (A) lateral, (C) medial views.
(B, E) CMNH 5698, left infragnathal, (B) lateral view, (E) closeup of marginal row of teeth. (D) CMNH 7888, anterior supragnathal,
anterolateral view. (F) CMNH 5230, right infragnathal, lateral view. (G) Gorgonichthys clarki (Claypole, 1892), CMNH 7129, left
infragnathal, lateral view. Larger unlabelled white arrows indicate the anterior direction. Abbreviations : bt.s, biting surface on
gnathal ; CMNH, Cleveland Museum of Natural History, Cleveland ; l.t., latest tooth to be added to the tooth row ; marg., marginal
tooth row ; med., medial tooth row or tusk ; symph., symphyseal tooth row or tusk. Scale bars=1.0 cm.

rows of teeth are present on the coccosteomorph infra-
gnathal, one located at the symphysis and a second pos-
teriorly along the dorsal jaw margin. A third medial row
may be present between these in some genera (Fig. 7H). We
interpret the point where these rows meet as the growth
centre and location of the first tooth primordium (see Smith,
2003) and from this the position of each tooth row on the
supra- and infragnathals is regulated. For example, on the
anterior and posterior supragnathals, the position of new
teeth is exactly reciprocated medially on the posterior pro-
cess (pr.post) on both the left and right supragnathals in taxa
such as Harrytoombsia and Compagopiscis (Fig. 7 A, B, F ; Miles
& Dennis, 1979 ; Gardiner & Miles, 1994).
In the supragnathal/infragnathal rows, the newest tooth
is added to a specific location at the end of the row and most
importantly, is formed away from the biting surface, and in
advance of use on this surface (Figs. 7, l.t, 11E, G–I, t3–t5).
These new teeth are inferred to form from separate pri-
mordia located only at these sites, developed from the orig-
inal or initial tooth primordium. The teeth erupt by
differential growth of bone, prior to their incorporation into
the functional biting surface (Fig. 7, bt.s), located on the
infragnathal between the symphyseal (symph.) and marginal
(marg.) tooth rows. Teeth from the third, medial row (med.),
if present, are also incorporated into this biting surface and
are better developed in certain taxa relative to others (com-
pare Fig. 7 H, L). In addition, the shape and polarity
(orientation) of the teeth is constant through the row (e.g.
Figs. 7A–H, 11 E, G–I), and the base of each tooth is closely
apposed to the adjacent one. It is noteworthy that original
12 Zerina Johanson and Moya M. Smith

Fig. 7. For legend see opposite page.

Origin and evolution of gnathostome dentitions 13

descriptions of these coccosteomorph gnathal plates by
Dennis and Miles (1980) consistently refer to ‘ teeth ’ and
‘ tooth rows’.
( ii ) Diversity and arrangement of structures in the coccosteomorph
dentition. The above observations apply to several types of
coccosteomorph dentition that otherwise function in differ-
ent feeding types. For example, the dentition on the supra-
gnathals of coccosteomorphs such as Harrytoombsia elegans
(Miles & Dennis, 1979) must have occluded with that on the
infragnathals, but strong shearing surfaces are not devel-
oped (Fig. 7 A–H). In Kimberleyichthys whybrowi (Dennis-Bryan
& Miles, 1983), a deep shearing surface is formed (Fig. 7K) ;
by comparison, the main biting surface of Bullerichthys fasci-
dens (Dennis & Miles, 1980) is flatter and represents a duro-
phagous, or crushing, dentition (Fig. 7 I, J). Discrete tooth
rows are readily observed on Harrytoombsia elegans and
Compagopiscis croucheri (Fig. 7 C) while in Kimberleyichthys why-
browi, most of the row has been worn away and incorporated
into the extensive shearing surface. However, two teeth are
visible dorsal to this surface (Fig. 7 K, l.t), produced prior to
incorporation into the bite. This was one of the criteria for
teeth produced within a dental lamina (Reif, 1982), and it is
clear that the teeth in Kimberleyichthys whybrowi are produced
in a similar manner. Interestingly, its predecessor in the
tooth row appears just functional at the biting surface
(Fig. 7K, larger arrow), indicating an ongoing, dynamic
process associated with growth of the gnathal element.
The anterior supragnathal of Bullerichthys fascidens shows
teeth being added to two separate rows (see Fig. 10 in
Dennis & Miles, 1980), but its posterior supragnathal, used
as a durophagous dentition (Dennis & Miles, 1980), is very
informative. Several rows of teeth are visible on the lateral
surface of the plate (Fig. 7I), continuing ventrally to the
biting surface. These lateral teeth are again produced out of
the bite, in advance of their use on this surface. More im-
portantly, the teeth are not added randomly, but are pro-
duced at a set location on the dorsal surface of the posterior
supragnathal. This is well below the oral surface, as new
teeth are embedded in the newest bone (Fig. 7 J, l.t) and here
attach to the palatoquadrate, where a small space for soft
tissue must have occurred for the tooth primordia of three
adjacent rows to develop.
( iii ) Juvenile dentitions: toothed rows. Juvenile or sub-adult
supragnathals and infragnathals have been described from
Incisoscutum ritchiei (Dennis & Miles, 1981), Eastmanosteus cal-
liaspis Dennis-Bryan, 1987 (see her Fig. 18) and Coccosteus
cuspidatus (Miles & Westoll, 1968). In Incisoscutum ritchiei, the
posterior supragnathal retains the three main tooth rows
identifiable in the adult form, with shorter rows associated
with the lateral and medial ones (see Fig. 13A in Dennis &
Miles, 1981). These additional rows are lost during growth
to the adult morphology (see Fig. 10 in Dennis & Miles,
1981). On the juvenile infragnathal, a distinct symphyseal
tooth is visible (see Fig. 12 in Dennis & Miles, 1981), as is a
row along the dorsal margin of the bone. New teeth are
added to the posterior end of this row, although only one
tooth is present in the symphyseal row. This symphyseal
tooth is the largest on the infragnathal and we consider this
to be a new tooth, representing the original primordium,
and site of subsequent addition to the symphyseal row tooth,
forming the adult dentition. Additionally, new denticles are
added along the inner face of the infragnathal, each with
associated bone of attachment (see Fig. 12 D in Dennis &
Miles, 1981). In Coccosteus cuspidatus, by comparison, juvenile
dentitions appear to have the same pattern of rows as seen in
the adult dentition but none of the denticles present in
Incisoscutum ritchiei (Miles & Westoll, 1968).
The morphology of the juvenile dentition is important
because it illustrates the early establishment of the symphy-
seal and marginal tooth rows on the infragnathal, and
lateral, medial and ventral rows on the supragnathal that
persist and generate new teeth into the adult stages (Fig. 7).
Similarity between the Incisoscutum ritchiei juvenile infra-
gnathal and the infragnathal of a brachythoracid arthrodire
similar to Buchanosteus fascidens has already been noted
(Young et al., 2001). Other ‘ primitive brachythoracids ’ (Carr,
1995), as well as certain pachyosteomorph arthrodires,
the Phlyctaeniida and the Phyllolepida (Fig. 4) also possess
upper and lower adult gnathalia in which new oral denticles
are added only at the margins of the existing denticulated
patch or area (Section III.b, c). The presence of these
denticles may represent a retained juvenile condition.
( iv ) Evidence in pachyosteomorph arthrodires for the presence of
teeth. In the pachyosteomorph arthrodires (Figs. 6, 8), den-
titions include both tooth rows and denticulated areas, the
latter occurring in the posterior region where the newest
tooth is added to the marginal row either medially or lat-
erally (Fig. 8 E, G, H, lat.dent, m.dent). The number of tooth
rows varies. For example, in the pachyosteomorph family
Dunkleosteidae, the supragnathals and infragnathals of
Dunkleosteus terrelli are characterised by well-developed
shearing surfaces (Fig. 6 ; Newberry, 1889). In both
Dunkleosteus terrelli and Gorgonichthys clarki (Claypole, 1892) a
large tusk dominates the symphyseal region of the infra-
gnathal (also present on the supragnathals), and a row of
separate symphyseal teeth is absent. However, a row of teeth

Fig. 7. Dental (gnathal) plates of coccosteomorph arthrodires. (A, B) Harrytoombsia elegans Miles & Dennis, 1979, WAM 70.4.254, left
and right anterior supragnathals, ventral (occlusal) view. (C) Compagopiscis croucheri Gardiner & Miles 1994, WAM 94.8.1, posterior
supragnathal, ventral view. (D, E) Harrytoombsia elegans, WAM 70.4.254, left suborbital plate with attached posterior supragnathal,
(D), medial (internal), (E) lateral views. (F) Harrytoombsia elegans, WAM 70.4.254, posterior supragnathal, medial view. (G) Gogopiscis
gracilis, WAM 94.5.1, posterior supragnathal, lateral view. (H) Gogopiscis gracilis, WAM 94.5.1, right infragnathal, medial view. (I, J)
Bullerichthys fascidens Dennis & Miles, 1980, WAM 70.4.259, right posterior supragnathal, (I) ventrolateral view, ( J) dorsal view. (K)
Kimberleyichthys whybrowi Dennis-Bryan & Miles, 1983, WAM 89.9.676, right anterior supragnathal, posterior view. (L) Bullerichthys
fascidens, WAM 70.4.259, right infragnathal, medial view. Abbreviations as in Fig. 6, also : gr.c, growth centre on gnathal plate ;
pr.post, posterior process on anterior and posterior supragnathals with accompanying teeth ; SO, suborbital plate ; WAM, Western
Australian Museum, Perth. Scale bars=1.0 cm (D and E, L), =0.5 cm (A and B, F–H, K), =0.25 cm (C, I, J).
14 Zerina Johanson and Moya M. Smith

Fig. 8. For legend see opposite page.

Origin and evolution of gnathostome dentitions 15

is present at the posterior edge of the shearing surface of
both the posterior supragnathal and the infragnathal, with
each tooth incorporated into this surface (Fig. 6 A–C, E, G),
comparable to taxa such as the coccosteomorph
Kimberleyichthys whybrowi (Fig. 7 K). The teeth in Dunkleosteus
terrelli are approximately equal in size along the tooth row,
and are evenly spaced within the row. The incorporation of
the anterior teeth into the shearing surface establishes a
polarity of tooth addition in this taxon and in others [e.g.
Gorgonichthys clarki, Fig. 6G] with these representing the
functional teeth and those at the end of the row as the newly
added or successor teeth. A medial row is represented on the
infragnathal by a second tusk positioned between the sym-
physeal tusk and the medial row of teeth. Ørvig (1980 a)
described the development of this tusk in substantial detail,
as ingrowing pleromic dentine, forming in response to wear
against the supragnathals (Fig. 12, tk).
Although the shearing surfaces and large tusks result in a
morphologically dramatic dentition for the Dunkleosteidae,
the length of the functional shearing surfaces is maintained
posteriorly by the addition of new teeth, as described above
for the coccosteomorph arthrodires. Other pachyosteo-
morph gnathals show even greater similarity to the cocco-
steomorph condition. For example, in Heintzichthys gouldii
(Newberry, 1885) and Gymnotrachelus hydei Dunkle & Bungart,
1939 (Fig. 8A–H ; Carr, 1991, 1994), the symphyseal and
marginal rows of teeth can be readily recognised on the
infragnathal (e.g. Fig. 8 E, F). On the posterior supragnathal
of Heintzichthys gouldii (Fig. 8 B) a row of widely separated
teeth crosses what appears to be the margin of the plate. The
teeth in the marginal row on the infragnathal are also evenly
spaced and nearly all the same height posteriorly, although
the teeth do become notably smaller anteriorly. Polarity
of tooth addition on the infragnathal is indicated by this
anterior decrease in size. As well, the thickness of the bone of
attachment (Fig. 8 A, b.att) is noticeably wider posteriorly,
associated with each new tooth, eventually becoming
thinner as it is incorporated into the infragnathal anteriorly.
Carr (1991) illustrated an ontogenetic sequence for
Heintzichthys gouldii (including Fig. 8 A, C, D) which shows
that teeth are eventually incorporated into a shearing sur-
face, as in the Dunkleosteidae. It appears that at some point
during this period of growth, tooth addition ceases com-
pletely, with the shearing surface maintained by ingrowing
pleromic dentine (Fig. 8 D).
The dentition of other pachyosteomorph taxa includes
denticulated areas. In taxa such as Gymnotrachelus hydei (Carr,
1994 ; Fig. 8 E–H) and Selenosteus brevis Dean, 1901 (Ørvig,
1980 a) this area occurs posteriorly, such that the marginal
row of the infragnathal continues posteriorly into this area.
Thus, it is more difficult to identify the newest tooth added
and the site of future tooth primordia. A comparable con-
dition is described below in the ‘ primitive brachythoracid ’
Antineosteus lehmani Lelièvre, 1984. Denticulated areas can
also occur along the medial, or lingual, side of the infra-
gnathal in pachyosteomorph taxa such as Protitanichthys sp.
(personal observations ZJ and MMS, 2002). The location
of this denticulated area is comparable to that described
above for the juvenile Incisoscutum ritchiei, and will also be
described in greater detail in Section III.(b) for Antineosteus
lehmani. Denticulated areas of this type occur in adult and
juvenile arthrodires, although in the coccosteomorph
arthrodires, they appear to be limited to the juvenile
morphology.
( b ) Other arthrodires: tooth rows and denticulated ‘ areas ’
The morphology of the dentition of these other arthrodires
is variable, and is discussed in reverse phylogenetic order
(Figs. 2, 4 ; Carr, 1995), from the phylogenetically basal
‘primitive ’ brachythoracids (e.g. Buchanosteus sp., Maideria
falipoui Lelièvre, 1995, Antineosteus lehmani) to the
Phlyctaeniida and the basal arthrodire group Actinolepida.
The Phyllolepida are described at the end of the section.
( i) ‘Primitive brachythoracids’ : teeth and denticles. The den-
titions of other brachythoracid arthrodires possess tooth rows
comparable to the coccosteomorph and pachyosteomorph
patterns, such as the ‘ primitive brachythoracids ’ (Fig. 4;
Carr, 1995) Maideria falipoui (Fig. 8 L, M ; Lelièvre, 1995),
Antineosteus lehmani (Fig. 9 ; Lelièvre, 1984) and a ‘ buchano-
steid ’ arthrodire described by Young et al. (2001). On the
anterior supragnathals of the ‘ buchanosteid’ and Maideria
falipoui (Fig. 8L, M), newer, larger teeth are arranged in
rows along the anterior margin (t.row, dent), surrounding a

Fig. 8. Dental (gnathal) plates of pachyosteomorph (A–H) and ‘primitive brachythoracid ’ (I–O) arthrodires. (A–D) Heintzichthys
gouldii (Newberry, 1885) (A, B) CMNH 8037 ; (A) left infragnathal, lateral view, (B) posterior supragnathal, lateral view. (C)
Heintzichthys gouldii, CMNH 8056, right infragnathal, lateral view, showing wear of tooth row. (D) Heintzichthys gouldii, CMNH 5728,
left infragnathal, lateral view, showing extreme wear of tooth row (bt.s) and formation of symphyseal tusk. (E–H), Gymnotrachelus hydei
Dunkle & Bungart, 1939 ; (E–G) CMNH 8051, right infragnathal, (E, F) medial view, (F) closeup of symphyseal tooth row and
anterior end of marginal tooth row, (G) lateral view. (H) Gymnotrachelus hydei, CMNH 8084, medial view of denticulated area on
posterior part of infragnathal. (I–K) ‘Saudi Arabian buchanosteid ’ MNHN ARB 239, (I) occlusal view anterior supragnathal, ( J, K)
medial and lateral views of infragnathal. (L–M) Maideria falipoui Lelièvre, 1995, headshield and anterior supragnathal plate in (L)
ventral view. (M) Natural break through tooth in tooth row (t.row), showing pulp cavity (arrow). (N–P) Holonema westolli Miles, 1971
WAM 95.6.09. (N) medial view of gnathal plate associated with the infragnathal. (O, P) postbranchial lamina, anterior view. (O)
entire lamina. (P) closeup of denticle rows near ontogenetic origin of lamina, indicated by larger white arrows in (O, P). (Q)
Incisoscutum ritchiei Dennis & Miles, 1981, AMF121767, closeup of denticles on postbranchial lamina. Abbreviations as in Figs. 5–7,
also : AMF, Australian Museum, Sydney ; b.att, bone of attachment ; dent, denticles on gnathal plate ; lam.marg, dorsomedial margin
of the postbranchial lamina where new denticles, either separate or in short rows, are generated ; lat.dent, m.dent, lateral and
marginal field of denticles ; MNHN, Museum National d’Histoire Naturelle, Paris ; t.pipe, ‘tooth pipe’ comprising dentition of the
basal arthrodire Holonema ; t.row, tooth row. Scale bars=1.0 cm in all ( J and K share one) except =0.2 cm (M), =0.5 cm (I, Q).
16 Zerina Johanson and Moya M. Smith

Fig. 9. For legend see opposite page.

Origin and evolution of gnathostome dentitions
posterior patch of denticles (see Fig. 6 in Lelièvre, 1995 ; and
Figs. 2, 3 in Young et al., 2001). A tooth row can be seen on
the infragnathals of the ‘ buchanosteid’ (see Fig. 2 C in
Young et al., 2001), with the largest tooth visible occurring at
the ventral part of the symphyseal region. A small patch of
denticles also occurs along the lingual face of the infra-
gnathal (see Fig. 4 A, B in Young et al., 2001 ; personal ob-
servations ZJ and MMS, 2001). This lingual area can be
seen in other buchanosteid taxa (e.g. an undescribed taxon
from Saudi Arabia), although on associated supragnathals of
these taxa, tooth rows are present alternating with edentu-
late areas (Fig. 8 I ; see Fig. 3 D–G in Young et al., 2001). On
the infragnathal a marginal tooth row is present, while
denticles can be observed both on the medial and lateral
faces of the infragnathal (Fig. 8 J, K, m.dent, lat.dent). This
also characterises the ‘ primitive ’ brachythoracid Antineosteus
lehmani, as described below.
Young et al. (2001, p. 675–676) describe a transformation
sequence or series between the ‘primitive tuberculate tooth
plates ’ of the new ‘ buchanosteid ’ and the more specialised
gnathal elements of eubrachythoracids, such as the cocco-
steomorphs described above. In this proposed evolutionary
sequence, the ability to produce enlarged teeth along the
margins of the gnathal plate (described as ‘denticles ’ by
Young et al., 2001) is retained. Subsequent loss of the pos-
terior ‘ denticle field ’ occurs in the ‘ buchanosteid ’ and
Maideria falipoui (Young et al. 2001, their Figs. 2, 3), to attain
the morphology seen in coccosteomorphs (Fig. 7) including
Coccosteus cuspidatus (Fig. 5, Miles & Westoll, 1968) or
Incisoscutum ritchiei (Fig. 11 A, E, G–I). Thus, Young et al.
(2001, see their Figs. 3, 4) suggest that tooth rows on the
anterior supragnathal of coccosteomorphs are homologous
to the anterior and lateral tooth rows of the brachythoracid
‘ buchanosteid ’ arthrodire. We agree with this interpret-
ation, although Young et al. (2001) referred to these as rows
of denticles, but we would maintain that coccosteomorph
dentitions possess ordered teeth showing the characteristics
described for the tooth rows or sets of other jawed ver-
tebrates. We do not currently know if they are also composed
of the same type of dentine, but each is added to only one
locus on the gnathal bone. Therefore, contrary to Young
et al. (2001) we would suggest that the anterior and lateral
row in their ‘ buchanosteid ’ and Maideria falipoui must also
represent teeth. As in the coccosteomorph tooth row, teeth
in the anterior row of the ‘ buchanosteid ’ supragnathals are
added to the (medial) end of the row (Young et al., 2001), are
larger in this position, and also have an associated bone of
attachment (personal observations ZJ and MMS, 2001). We
noted that this bone of attachment can be identified and
associated with each tooth in the row. As noted above for
the pachyosteomorph arthrodire Heintzichthys gouldii, the
bone appears to be thickest in association with the newer
Fig. 9. Infragnathals of the ‘primitive brachythoracid’ (Fig. 4) Antineosteus lehmani Lelièvre, 1984. (A–K) MNHN MCD 76 (includes
both left and right infragnathals). (A) Right infragnathal, occlusal view, (B) medial view, (C) lateral view. (D) Closeup of medial
denticles. (E–K) Left infragnathal. (E) Occlusal view, (F–G) closeup of symphyseal tooth row, (H) Closeup of marginal tooth row
(ridge), (I–J) lateral view. (K) occlusal view of separate piece of left infragnathal showing denticulated area posteriorly. Abbreviations
as in Figs. 6, 8, also : r.ar, resorption area. Scale bars=1.0 cm (A, B, E, I), =0.1 cm (C), =0.5 cm (F) and =0.2 cm (D, G, H, J).
17
teeth but thinner along the row towards the oldest tooth, as
this bone is remodelled into the main part of the gnathal
bone. The addition of new larger teeth to the end of
the tooth row can also be seen on the infragnathals of the
‘buchanosteid ’ (Young et al., 2001, see their Fig. 2C). We
consider that this may relate to the symphysial tooth row,
but is rather longer than in most taxa. In Maideria falipoui,
quite large new teeth are seen at the lateral margin and a
natural break shows a large pulp cavity in the teeth of this
row (Fig. 8M).
The infragnathal of Antineosteus lehmani, another ‘primitive
brachythoracid ’ (Fig. 4), is dominated by areas of denticles,
but one prominent feature is a marginal ridge along the
dorsal edge of the infragnathal (Fig. 9A, I, marg.). Nothing is
known of the upper gnathal elements for Antineosteus lehmani.
This elongate ridge is aligned with separate teeth, anterior,
or symphyseal in position (marg., marg./symph.). The pro-
cess by which these teeth are incorporated into the marginal
ridge during growth (forming the functional biting surface)
would seem to involve tooth addition at the anteriormost
part of the infragnathal (at the symphysis). In addition to
these teeth, new denticles are added to the medial (lingual)
side of the infragnathal (Fig. 9 B, D, H, m. dent), although a
smaller number also occur on the lateral surface (Fig.
9C, I, J, lat.dent). There is no clear arrangement or pattern
to the addition of these denticles, but at least medially, the
newest would appear to be added strictly to the margin of
the existing denticulated area, surrounded by well-devel-
oped bone of attachment (Fig. 9 B, D, b.att). This bone forms
a distinct pedestal around the base of the denticle.
Roughened areas occur just lateral and medial to the mar-
ginal tooth ridge (Fig. 9 H–J, r.ar) and would appear to be
linked to the resorption of the bone of the infragnathal, re-
lated to overall growth. In this way, lateral and medial
denticles are incorporated into the bone of the infragnathal
during growth and into the marginal biting ridge, which
appears to be flanked by regions of ongoing bone remodel-
ling. Comparable areas of resorption have been observed on
gnathal bones of certain coccosteomorph arthrodires, as
described below (Section IV.4). Only a histological study
will confirm these details of growth and remodelling.
( ii ) Phlyctaeniida : denticle fields. Observations of extensive
denticulated areas apply to other taxa assigned to the
Arthrodira, for example, members of the Phlyctaeniida
(Figs. 2, 4). The dentition of these is best represented by
Dicksonosteus arcticus (Fig. 10H ; Goujet, 1984 a ; Smith &
Johanson, 2003b) with a well-preserved posterior supra-
gnathal. Addition of new denticles occurs at the margins
of the gnathal plate and there is also a size gradation across
the supragnathal, so that the newly added denticles at vari-
ous positions along the plate margins are readily dis-
tinguished from their smaller predecessors. This represents a
18 Zerina Johanson and Moya M. Smith

Fig. 10. For legend see opposite page.

Origin and evolution of gnathostome dentitions 19

non-shedding condition or statodont dentition, although
denticles, rather than teeth, are involved. The smaller den-
ticles are situated closer to the centre of ossification of the
supragnathal, representing the point from which growth
progressed, now the functional biting surface. The newest
denticles are added outside this surface and overlap the
margins of the gnathal bone. We suggest this is an example
of a common morphological genetic programme in a hier-
archy shared with the more derived forms possessing teeth,
described above.
( iii ) Actinolepida : tooth addition. The final arthrodire group
to be considered is the Actinolepida (Figs. 2, 4). The den-
tition associated with the actinolepid infragnathal is nearly
identical to the coccosteomorph condition, with a row of
teeth at the symphysis and a second marginal row extend-
ing posteriorly (Denison, 1958; Dineley & Liu, 1984;
Mark-Kurik, 1985). As described for the coccosteomorph
dentition, the newest teeth are added at the base of the
symphyseal row, and posterior to the marginal row.
Undescribed actinolepid gnathals of Aethaspis from the
Water Canyon Formation, Utah show distinct teeth added
to rows. It is clear that the newest and largest teeth are
added medially to three tooth rows on the infragnathal
(Fig. 10A–C, black arrows ; Fig. S1A in Smith & Johanson,
2003 b). These decrease in size anteriorly, as the older pre-
viously added teeth are incorporated into the functional
biting surface and become worn (Fig. 10A). It has not been
possible as yet to investigate the histology of these speci-
mens. Denticles are not associated with this dentition,
as opposed to the dentitions of Antineosteus lehmani and
pachyosteomorph arthrodires such as Gymnotrachelus hydei
[but see Denison (1958, his Fig. 101B)]. Supragnathals
have been described for the actinolepid Actinolepis spinosa
(Fig. 10D, ASG, PSG ; Mark-Kurik, 1985) including an-
terior and posterior ‘ dental fields ’. Graded size sequences
can be seen for the teeth included in these fields, and they
conform best to the tooth rows described above.
( c) Phyllolepida : denticle fields
The Phyllolepida have been excluded from the Arthrodira,
based on the putative absence of a posterior supragnathal
(Denison, 1978 b ; Carr, 1995), but are included in the
Arthrodira in the cladogram shown in Figure 4 (and in
recent analyses of Goujet & Young, 2004, their Fig. 1). As
described above in the Phlyctaeniida, new denticles are
added to the margins of the phyllolepid anterior supra-
gnathal (Fig. 10E–G) and there is a gradation in size across
the gnathal plate (Long, 1984; Ritchie, 1984). In Placolepis
budawangensis Ritchie, 1984, the denticles can form rec-
ognisable rows across the gnathal surface (Fig. 10 F, G),
although these are less distinct in other phyllolepids such as
Austrophyllolepis ritchiei Long, 1984 and Austrophyllolepis youngi
Long, 1984 (Long, 1984, his Figs. 5, 18 ; also Fig. 10E for an
new undescribed Australian taxon). New denticles are not
added between or among their predecessors on the gnathal
bone, and there is no evidence of superimposition of newer
denticles above older. The infragnathal is relatively narrow
compared to the supragnathal, but again, new denticles are
added marginally with smaller, worn denticles in the middle
of the plate. Thus, newly formed marginal denticles are
added to a statodont dentition out of the biting surface.
Comparable with the phlyctaeniid arthrodires, the location
of these new denticles, at the gnathal margin, is partially
regulated, and can be considered part of the developmental
morphological hierarchy relative to the tooth rows described
for a variety of brachythoracid and actinolepid arthrodiran
taxa.
The dentition of the Arthrodira provides the best struc-
tural and histological evidence for the presence of teeth
comparable to those possessed by other jawed vertebrates.
Among more phylogenetically basal placoderm groups
(Fig. 2), teeth are absent, and the rounded or pointed den-
ticles described for the Arthrodira may only be present in a
limited number of taxa (Gemuendina Traquair, 1903). These
groups, the Acanthothoraci, Antiarchi and Rhenanida, will
be discussed in turn below.
( d ) Acanthothoraci : supragnathal plates
The Acanthothoraci are known from very well preserved
head- and trunkshield materials (e.g. Stensiö, 1969 ; Ørvig,
1975 ; White, 1978; Young, 1980), but the dentition is vir-
tually unknown. Recently however, a single specimen of
Romundina sp. has been discovered by D. Goujet (Paris)
preserving a pair of anterior supragnathal plates articulating
to the ethmoidal region of the braincase. These anterior
supragnathals are covered in denticles that differ in their
pattern of arrangement from the tubercles covering the
adjacent, inturned face of the rostral plate of the headshield

Fig. 10. Dental (gnathal) plates of a variety of placoderms. (A–D) Actinolepida. (A–C) Aetheaspis sp. (A) Left infragnathal, lateral view
showing marginal tooth row. (B) Right infragnathal, medial view showing symphyseal row. (C) Infragnathal showing at least three
separate tooth rows (arrows). (D) Actinolepis spinosa (drawing taken from Mark-Kurik, 1985, Pi 1094b). (E, F, G) Phyllolepida,
supragnathal plates, occlusal view (E) Phyllolepida n. gen., n. sp., AMF96756. (F, G) Placolepis budawangensis Ritchie, 1984. (F) AMF
61920 ; (G) AMF 61761 (both from Ritchie, 1984). (H) Dicksonosteus arcticus Goujet, 1975 (Phlyctaeniida), MNHN SVD 114, posterior
supragnathal, occlusal view (from Goujet, 1984 a). (I, J) Antiarchi, suborbital plates in oral cavity, ventral surface, showing continuity
of ornamentation with external head and trunkshield. (I) Phymolepis cuifenshanensis Young & Zhang, 1996, IVPP.V9059.1.
( J) Bothriolepis sp., CPC 25205 (from Young, 1984). (K, L) Jagorina pandora Jaekel, 1921 (Rhenanida), MB.f. 510.3. (K) Infragnathal,
anteromedial view. (L) occlusal view of biting surface showing small polygonal units crowded onto surface. Abbreviations as in Fig. 7,
except in D where abbreviations as in Fig. 5. Scale bars=0.5 cm (A, B, E, J), =0.2 cm (C, D, H), =1.0 mm (I), =0.8 cm (K) and
=1.0 cm (F, G, I). Abbreviations : CPC, Commonwealth Palaeontological Collection, Canberra ; IVPP, Institute of Vertebrate
Palaeontology and Palaeoanthropology, Beijing ; MB, Museum für Naturkunde, Humboldt Universität, Berlin ; Pi, Institute of
Geology, Estonian Academy of Sciences.
20 Zerina Johanson and Moya M. Smith

Fig. 11. Growth and remodelling in teeth and gnathal bones in scanning electron micrographs of natural growth and wear surfaces
of gnathal bones from Devonian fossils of Gogo in Western Australia. All arranged with the oral surface uppermost independent of
body position. (A, B) Incisoscutum ritchiei AMF 95644, right anterior supragnathal. Lateral surface in A shows new tooth addition
(arrows) below the abrasion surfaces (^^), and above a vascular bone surface with small areas of scalloping due to localised resorption
(**), this bone resorption is seen at higher magnification in B. (C, D) Goujetosteus sp. (=Torosteus sp. of Gardiner & Miles, 1990) WAM
88.6.3, left anterior supragnathal. (C) Medial face of natural cutting edge (c.e) with abrasion marks and below this are clear growth
Origin and evolution of gnathostome dentitions 21

(D. Goujet, personal communication ; see also Smith & A B

Johanson, 2003a). Thus, a distinction can be made between
the oral and external skin denticles in this basal placoderm
group. The morphological gradation between external and
oral denticles identified for the Heterostraci by Purnell
(2001) is not observed. The supragnathal denticles are
however quite different and distinct from arrangements on
other gnathal plates described above. The denticles appear
to be smaller towards the growth centre of the supragnathal,
located in the middle of the bone, as described for the
statodont, denticulated dentitions of the Phlyctaeniida and
Phyllolepida, although the denticles themselves are some-
what elongate, rather than rounded (D. Goujet, undescribed
material). Despite the lack of dental material available for
study, the Acanthothoraci represents the most basal placo-
derm group in current phylogenies and shows that oral el-
ements are not added to a defined and restricted number of
tooth rows, as described for the teeth of the Arthrodira. This
is an important and key observation for the origin of teeth in
the placoderm phylogeny, supported by the next most basal
groups in the placoderm phylogeny, the Antiarchi and
Rhenanida.
( e ) Antiarchi and Rhenanida : external dermal elements in the dentition
In the Antiarchi (Fig. 2), the infragnathal is an elongate,
S-shaped structure, with an anteromedial biting region
either edentate (e.g. Johanson, 1997) or supporting a
roughened bone meshwork (Young, 1984). The upper
feeding structures are formed from suborbital plates of the
headshield that have become positioned within the mouth
(Fig. 10I, J ; Young, 1984). The suborbital plate comprises
the cheek of other placoderm groups (Denison, 1978 b).
Antiarch suborbitals are best known for Bothriolepis sp., based
on specimens from the Gogo Formation of Western
Australia (Young, 1984). The palatoquadrate lines the
internal surface of the suborbital and contacts the endo-
cranium at possibly three points. The posterior supragnathal
of the Arthrodira also articulates to the palatoquadrate.
However, the antiarch suborbital cannot be considered
homologous to the posterior supragnathal as both structures
occur in arthrodires (Denison, 1978b), failing the conjunc-
tion test of homology (Patterson, 1982).
The ventral, external surface of the suborbitals of
Bothriolepis sp. shows an open bony texture, comparable to
the external surface of the dermal plates covering the head
t4
sy.t.5 t5
t1
sy.t.1
tk at.
C
c.e. t1
t6
sy.t.1
sy.t.5
Fig. 12. Plourdosteus canadensis Woodward, 1892, diagrams of
growth and wear in the three gnathal bones. (A) Anterior
supragnathal (ASG). (B) Posterior supragnathal (PSG). (C)
Infragnathal (IG) (modified from Figs. 34, 39, 43 in Ørvig,
1980a, actual arrangement unknown). The direction of tooth
addition (thin arrows) and removal by wear of the pleromic
dentine tissues (thick arrows) as proposed by Ørvig, 1980a.
Teeth (sy.t.1–t.5) are added to each of the symphyseal rows, to
the posterior rows of the PSG (t1–t4) and IG (t1–t6), and to the
lateral row of the PSG (t1–t5). Teeth show wear through at-
trition (at., attrition facets) and add to the biting surface, or
cutting edge (c.e, hatched). Wear is accommodated by internal
growth of the pleromic dentine as a type of compensatory
growth. Where the cutting edge is enhanced as a tusk (tk) this is
formed by internal growth of extra hard pleromic dentine, this
growth is indicated by the central stippled areas on the ASG,
PSG, and IG.
and trunkshield (Young, 1984 ; Fig. 10J). This is also dem-
onstrated by the suborbitals of the antiarch Phymolepis cui-
fenshanensis Young & Zhang, 1996, where the external
surface is covered by the same scattered dermal tubercles as
occur on the external headshield plates (Fig. 10I). Phymolepis
cuifenshanensis is assigned to the Yunnanolepidoidei, a taxon

bands (arrows ; see Ørvig, 1980 a, also Fig. 12). (D) Cutting edge surface, specimen etched with 1 N HCl for 1 min to reveal structural
details of pleromic dentine, biological infilling of vascular dentine spaces, and importantly a reversal line (arrows) where new tissue
has been deposited onto the previous resorption surface in the process of remodelling through tissue addition (top edge is the
abrasion surface of C). (E–G) Incisoscutum ritchiei AMF 95644, left infragnathal, medial view of posterior tooth row (t1–t4) and cutting
edge (c.e) above an extensive resorption surface (arrows) with deep resorption pits of osteoclastic action as a natural biological
remodelling process. Higher magnification (F) shows that the smooth walls of the vascular canals are unaffected by this process. (G)
Medial view of unetched natural surfaces of symphyseal tooth row (t3), shows extensive active resorption (arrows) and the beginning
of redeposition of tissue (**), onto a resting bone surface. (H) Incisoscutum ritchiei AMF 121767, right infragnathal, new tooth (t3) added
to symphyseal tooth row on the new bone surface, above is a smooth coating tissue (c.d) assumed to be a type of dentine (shown as
the surface layers in Fig. 19A, E). (I) Incisoscutum ritchiei AMF 95644, right anterior supragnathal, occlusal view of symphyseal tooth
row (t1–t5) the degree of wear compares directly with the wear facets in the diagram (Fig. 12), biting surfaces of the tusk (tk) and
cutting edge (c.e).
22
Fig. 13. Gemuendina stuertzi (Rhenanida). (A, B) KGM 1983/306, (C) KGM 1983/308. (D) KGM 1983/307. (A) Headshield and
anterior trunkshield, dorsal view. (B, C, D) Closeup views showing denticulated infragnathals (e.g. smaller white arrows in B).
Abbreviations : KGM, Karl-Geib Museums (now Schlossparkmuseum), Bad Kreuznach, Germany. Scale bars=1.0 cm (A),
=0.5 cm (B–D).
occupying the basal node within the antiarch clade (Zhu,
1996). Thus, the presence of the suborbital as a feeding
structure within the oral cavity occurs throughout the group
(see also Young, 1984; Zhu, 1996; Johanson, 1997). In
Bothriolepis sp., the posteroventral margin of the suborbital is
smooth, with small denticles located along the biting edge of
the plate (Stensiö, 1948; Young, 1984; Fig. 10 J). This
margin is completely smooth in Phymolepis cuifenshanensis and
in taxa such as Remigolepis walkeri Johanson, 1997. The
Antiarchi provides an intriguing example of a group in
which external dermal structures have been co-opted into
the dentition and one in which the external ornamentation
of the headshield can be said to grade into the oral cavity.
However, neither this ornamentation, nor the suborbital
plate, are representative of teeth comparable to those de-
scribed for the Arthrodira, instead it would seem to be an
alternative solution to recruit dermal ornament to serve as
the functional dentition.
A comparable contribution of the suborbital to the upper
dentition may occur in Nefudina qalibahensis, a member of the
Rhenanida (Lelièvre et al., 1995), although the plate itself is
not situated within the oral cavity as it is in the Antiarchi.
The ventral margin of the suborbital of Nefudina qalibahensis is
covered by several large, randomly positioned denticles.
These were said to be potentially related to the absence of
supragnathals (Lelièvre et al., 1995 ; also Stensiö, 1969;
Zerina Johanson and Moya M. Smith
Goujet, Janvier & Racheboeuf, 1993), implying that they
were acting as part of the upper biting apparatus.
Otherwise, separate supragnathals appear to be absent in
the entire group. The biting surface of the infragnathal of
the rhenanid Jagorina pandora Jaekel, 1921 (Fig. 10 K, L ;
Young, 1986) is covered in small units polygonal in
appearance. These were said to be comparable to the small
plates (tesserae) covering the external surface of the head-
shield, randomly distributed and crowded onto the biting
surface (Stensiö, 1959, 1969; Young, 1986; Young et al.,
2001). Given the damage to the specimen (Fig. 10L), it is
very difficult to discern addition of new dentition units to the
biting area. The only other rhenanid from which the den-
tition is known is Gemuendina stuertzi Traquair, 1903 (Fig. 13 ;
plate 2 in Gross, 1963 ; Young, 1986, his Fig 10 E after
Gross 1963), again only from infragnathals, although entire
specimens are preserved. The dentition associated with
the infragnathal appears arranged in ordered rows across
the biting surface (Fig. 13 A, B; Gross, 1963, his plate 2),
much more so than is the case for Jagorina pandora Jaekel,
1921. These are featured also in a radiograph (Case, 1992)
in which each denticle is seen as separate. A closeup of this
region (Fig. 13 B) does show some ordering into rows (small
white arrows), with a larger arrow marking a row of what
appear to be larger denticles, perhaps part of the symphyseal
row. However, other specimens (Fig. 13C, D) show a more
Origin and evolution of gnathostome dentitions
random arrangement, comparable to the denticle mor-
phology in the Phyllolepida (Fig. 10E). In Gemuendina stuertzi,
these are also likely to be denticles rather than teeth, and
do not appear to be related to external dermal structures
but are defined as oral denticles (Gross, 1963). Thus, the
group Rhenanida includes a notable range of dentition
morphologies.
The three phylogenetically basal groups of placoderms
(Figs. 2, 4) possess a variety of dental morphologies, and
although the antiarch and rhenanid dentition has been well
described, that of the Acanthothoraci has not. Interestingly,
the Antiarchi and two taxa assigned to the Rhenanida
(Nefudina and Jagorina) may utilise external dermal structures
(suborbitals and tesserae) in their dentitions. Incorporating
this character into new phylogenetic analyses of the
Placodermi may result in these taxa being resolved to the
basal nodes of the group, rather than the Acanthothoraci.
Within these taxa, only the infragnathals of Gemuendina
stuertzi may show rows of denticles comparable to those
described above for the Phyllolepida and Phlyctaeniida.
( f ) Other denticles in the oral cavity : parasphenoid and paraotic plates
Other than the paired supragnathals and infragnathals,
dermal bones of the placoderm oro-pharyngeal cavity are
rare elements of the splanchnocranium. Those restricted to
the pharygneal region are discussed in Section III.2. Stensiö
(1963, 1969) suggested that the placoderm supragnathals
were homologous to the osteichthyan vomers and palatino-
pterygoids, but Young (1986) rejected this, noting that
these dermal elements did not show strong enough topo-
graphic correspondence to warrant homology. The only
other dermal bone in this region of the oro-pharyngeal
cavity is the parasphenoid, although in taxa such as
Nefundina (Rhenanida, Lelièvre et al., 1995), denticulated
paraotic plates are present posterior to the parasphenoid
and serve to floor the notochord.
Most of the known placoderm parasphenoids are from
the Arthrodira, with the only exceptions being the para-
sphenoids of Nefudina qalibahensis, Kosoraspis peckai Gross, 1959
(Acanthothoraci) and possibly an undescribed Bothriolepis sp.
(Antiarchi) from the Gogo Formation (Dennis-Bryan, 1995).
In general, the parasphenoid is pierced by a single, or pair
of, buccohypophyseal foramina. In some taxa, a shallow
transverse groove extends from the hypophyseal foramina to
the lateral edge of the parasphenoid. Beyond these simi-
larities, the placoderm parasphenoid shows a variety of sizes
and shapes and extent of denticulation across the ventral
surface (Dennis-Bryan, 1995). The denticles on the para-
sphenoid show no particular organisation or patterning, but
notably, differ morphologically from the tubercles on the
external surface of the headshield.
In adult jawed vertebrates, the hypophyseal gland marks
the boundary between the oral and pharyngeal cavities.
Because the formation of the hypophysis involves both
ectodermal (Rathke’s pouch) and endodermal (Sessel’s organ)
contributions, a boundary between these epithelia can also
be recognised, even though the original boundary between
oral and pharyngeal cavities is lost during ontogeny. The
buccohypophyseal foramen in the parasphenoid of a variety
23
of fossil taxa allows for the identification of an ectodermal-
endodermal boundary in these ; in sharks the hypophyseal
foramen is closed over, but a parasphenoid-like concen-
tration of denticles also permits this boundary to be ident-
ified.
A patterning influence of the endodermal-ectodermal
boundary has been suggested for all elements of the
splanchnoskeleton (reviewed in Smith, 2003, and see below)
as well as for the organised denticles on the postbranchial
lamina at the rear of the pharyngeal cavity (Johanson &
Smith, 2003 ; Section III.2.b). This boundary may also oc-
cur within the gill slits (Fig. 3) and denticles in this region in
a variety of sharks show clear organisation into rows along
the branchial arches (Nelson, 1970b). Although the influ-
ence of these boundaries must currently be hypothetical
until endodermal markers for use in in situ hybridisation
are better developed, the boundary associated with the
hypophysis is well established.
(2 ) Pharyngeal cavity : presence of pharyngeal
denticles
Although the gill arches of placoderms are very poorly
known (the rhenanids being an exception), all placoderm
taxa (Figs. 2, 4) show evidence for patterned or organised
denticles within the pharyngeal cavity (Johanson & Smith,
2003). This occurs in a more caudal but comparable anat-
omical region to that of organised denticle whorls described
for the thelodont Loganellia scotica (Fig. 3B ; van der Brugghen
& Janvier, 1993 ; Smith & Coates, 1998). Although neither
denticles nor dermal bony plates are observed on the phar-
yngeal arches and there are only two taxa possessing gill
rakers, a denticle cover is prominent in all other taxa on the
rear wall of the placoderm gill chamber. This is formed by
the medial aspects of the dermal plates associated with the
trunkshield and known as the postbranchial lamina (Fig.
3D, PBL). These denticles differ morphologically from the
external denticles or tubercles comprising the dermal orna-
ment of the head and trunkshield armour, and differ sig-
nificantly in their pattern (formed into rows). These
structural differences allowed us to infer different develop-
mental processes involved in internal and external denticle
formation and patterning (Johanson & Smith, 2003), in
terms of the participation of different cell lineages (ectoderm
versus endoderm and trunk versus cranial neural crest).
( a ) Gill arches and skeletal components
Dermal elements covering the gill arches have been de-
scribed for a variety of chondrichthyan, acanthodian and
osteichthyan taxa, including gill rakers and bony plates
covered by denticles or teeth (Nelson, 1969; 1970 a, b ;
Miles, 1971 ; Clemen et al., 1998; Grande & Bemis, 1998;
Huysseune, 2000 ; Wacker, Bartsch & Clemen, 2001).
Placoderm gill arches have been described from the
Ptyctodontida (Ørvig, 1960, 1962 ; Forey & Gardiner, 1986;
Long, 1997), a very limited number of arthrodires (Stensiö,
1963, 1969) and the Rhenanida (Gross, 1963 ; Stensiö, 1963,
1969). Of these, gill rakers are present on the branchial
arches of the rhenanids Jagorina pandora and Gemuendina stuertzi
24 Zerina Johanson and Moya M. Smith

Fig. 14. For legend see opposite page.

Origin and evolution of gnathostome dentitions 25

(Gross 1963), but bony plates and denticles have not been
described. In Jagorina pandora (Fig. 14 G, black arrows), only
the bony bases of the gill rakers are preserved, while the
pointed rakers are visible in X-rays of Gemuendina stuertzi.
These are both positioned at distinct and evenly spaced
positions along the gill arch itself, particularly noticeable
along the preserved gill arches of Jagorina pandora, and in-
terestingly the bases decrease in size medially along the row
in this taxon.
The organisation of these gill rakers at particular locations
(and the possible size gradation) is suggestive of a skeletal
patterning mechanism within the pharyngeal cavity in ad-
dition to the iterative gill supports. In placoderms lacking
preserved gill cartilages, patterning is evident in the den-
ticulate ornamentation along the postbranchial lamina
(Johanson & Smith, 2003).
( b ) Postbranchial lamina and denticle pattern
The postbranchial lamina forms the rear wall of the gill
chamber in placoderms (Figs. 8 O–Q and 14A–F, H),
osteichthyans and rarely in acanthodians (e.g. Diplacanthus
crassimus Duff, 1842 ; Denison, 1978 b ; White, 1978;
Gardiner, 1984a ; Zhu et al., 1999; Zhu & Schultze, 2001).
Stem-tetrapods with digits, such as Acanthostega gunnari Jarvik,
1952 and Whatcheeria deltae Lombard & Bolt, 1995 also pos-
sess small postbranchial laminae (Lombard & Bolt, 1995;
Coates, 1996). Although forming the rear of the gill chamber,
the lamina itself is formed as a medially directed flange of
bone from the anterior trunkshield plates in placoderms and
the dermal pectoral girdle in osteichthyans and stem-
tetrapods (cleithrum and clavicle). The homology of these
bones of the shoulder girdle has been discussed by a variety
of authors (Stensiö, 1959; Forey, 1980 ; Gardiner, 1984 a;
Zhu & Schultze, 2001). In nearly all placoderms, the lamina
is covered in denticles that are morphologically different,
being triangular in shape or some variation on this (Fig. 14),
from the tubercles covering the external surface of the
head and trunkshield plates, which are generally rounded
(Figs. 14 H, 15 B). Further, these triangular denticles of
the laminae are ordered into staggered, offset files (e.g.
Romundina stellina Ørvig, 1975 (Acanthothoraci), Nefudina
qalibahensis (Rhenanida), Antineosteus lehmani (‘ primitive
brachythoracids ’), Eastmanosteus calliaspis (coccosteomorph
arthrodire)), or into separated rows extending across the
laminar surface. The latter morphology occurs in Bolivosteus
chacomensis Goujet, Janvier & Suárez-Riglos, 1986
(Rhenanida), Yunnanolepis chii Liu, 1963 (Antiarchi),
Rhynchodus eximius ( Jaekel, 1919) (Ptyctodontida),
Dicksonosteus sp. (Phlyctaeniida), Holonema westolli Newberry,
1889 (Brachythoraci ; Fig. 8O–Q) and Harrytoombsia elegans
Miles and Dennis, 1979 (Eubrachythoraci)) (Miles, 1971;
Zhang, 1978 ; Chang, 1980 ; Goujet, 1984 a ; Goujet et al.,
1993 ; Lelièvre et al., 1995 ; Johanson & Smith, 2003).
Denticles are added either individually to the files, or in
shortened rows at the dorsomedial margin of the lamina
(Figs. 8 O–Q, 14 A, D, F, lam.marg), but not within or
among the denticles already present on the lamina. It would
appear that these denticles form as the bone of the lamina is
added to the dorsomedial margin and a new surface for their
attachment becomes available. The denticles themselves are
attached to the surface of the lamina, but do not form from
within the bone of the lamina. When denticles are lost, for
example, during preparation, the lamina beneath is either
smooth or shows a very shallow pit, representing the loss of
the denticle and its bone of attachment (see Fig. 8 C in
Johanson & Smith, 2003). Although the external denticles of
the head and trunkshield can also be organised into rows,
the differing morphologies externally and on the post-
branchial laminae suggest development from different em-
bryonic cell layers.
The actual distribution of ectoderm and endoderm within
the oral and pharyngeal cavities still needs to be demon-
strated experimentally, even in ‘ model ’ animals such as the
zebrafish. However, structural evidence for the topographic
position of a boundary between these cell layers is provided
by the position of the hypophyseal opening in the para-
sphenoid bone (Section III.1.f). In Loganellia scotica, patterned
denticle whorls present on the inner side of the branchial
arches place these whorls within the pharyngeal cavity and
under the presumptive influence of endoderm. Notably,
early researchers considered the pharyngeal denticles of
elasmobranchs and pharyngeal teeth of Cyprinus carpio to be
derived from the endoderm (Cook & Neal, 1921 and
Edwards, 1929, both cited in Sellman, 1946). In placo-
derms, the internal position of the postbranchial lamina,
topographically within the gill chamber or pharyngeal cav-
ity, suggests this is also under the influence of embryonic
endoderm. The position of an ectodermal-endodermal
boundary in placoderms can be predicted at the ventro-
medial (Fig. 14D, H, larger arrows), or ventrolateral aspects
of the postbranchial lamina (Fig. 14 A, larger arrow). This
boundary is indicated by a change in denticle patterns
between the lamina internally and the external surface of
the interolateral plate, indicated by a single row of closely
packed denticles of identical size and shape (Fig. 14 H,

Fig. 14. (A–C, E) Campbellodus decipiens Long, 1997 (Ptyctodontida). (A) WAM 86.9.672, anterior lateral plate with postbranchial
lamina (PBL) covered in rows of denticles ; arrow marks the putative origin of ectodemal-endodermal boundary. (B) denticles on
dorsalmost part of PBL with certain denticles showing differences in orientation from the main rows. (C) Denticles from middle of
PBL. (E) Denticles from ventral and lateral parts of PBL. (D, F, H) Antineosteus lehmani Lelièvre, 1984, MNHN MCD 76. (D)
Postbranchial lamina, anterior view, larger arrows mark the successive growth stages of the lamina margin. (F) Closeup of denticles,
showing dorsomedial margin (lam.marg) along which new denticles are added. (H) MNHN MCD 76, postbranchial lamina (PBL)
and interolateral plate (IL), showing differences between rounded tubercles on the IL and triangular denticles on the interolateral ;
arrows mark the junction between the two types. (G) Jagorina pandora Jaekel, 1921, MB.f. 510.3, ventral gill arches showing bases of gill
rakers (black arrows) along arch surface. Abbreviations as in Fig. 8 : dent, denticles (pharyngeal) across anterior face of PBL ; IL,
interolateral plate of trunkshield ; tu, tubercles covering trunkshield. Scale bars=1.0 cm, except for =0.25 cm (C), =0.20 cm (B, E, F).
26
Coates, 1996, IL, large arrows). The dorsomedial/
ventrolateral margin of the postbranchial lamina represents
the site where denticles are generated (Fig. 14D, F, lam.
marg) and as this margin grows away from the original ecto-
endodermal boundary, it would still be covered by endo-
derm and continue to generate an endoderm-type pattern of
denticles. We suggest that epithelial signals were provided
here to establish the distinctive pharyngeal pattern for den-
ticle initiation at this site, especially their spacing, sequence
and timing of addition. The difference in shape, size and
arrangement between these denticles and dermal denticles
in placoderms is particularly well illustrated in interolateral
plates of Antineosteus lehmani and Campbellodus decipiens Long,
1997 (Ptyctodontida) (Fig. 14). Interestingly, in Campbellodus
decipiens, it appears that as the individual becomes older the
denticle patterning is less controlled, especially at the margin
now distant from the original boundary. For example, the
denticles at the latest generative margin, particularly those
dorsally, are no longer oriented into clear rows (Fig. 14B).
IV. A DEVELOPMENTAL MODEL FROM
PHYLOGENETIC PATTERN
Phylogenetic data potentially record the earliest manifes-
tations of a developmental module, namely that responsible
for producing tooth sets in gnathostome dentitions. One
example discussed here and dependent on accepted phylo-
genies is whether, or not, the developmental module
underlying regulation of tooth sets is conserved, or con-
vergently assembled. We have presented phylogenetic data
to propose a common, hierarchical morphogenetic pro-
gramme for placoderm dentitions. This is based on a para-
digm for tooth sets as part of an internal splanchnoskeleton
dependent on endoderm for their early induction.
(1 ) Ectodermal against endodermal patterning
Previously, Smith & Coates (1998, 2001 ; also Smith, 2003)
suggested that the position of the boundary between the
ectoderm and endoderm at the oro-pharyngeal membrane
was important to understand the observed differences be-
tween dermal denticles and teeth. They emphasised the
classic experiments in amphibians (Sellman, 1946) which
demonstrated the dependence of tooth formation on endo-
derm for induction as part of the genetic regulation for both
initial tooth loci and for replacement teeth. Compared to
those in the oro-nasal cavities the different observable pat-
tern of both arrangement and addition of the pharyngeal
denticles in the thelodont Loganellia scotica, emphasised the
significance and dependence on oral endoderm (Smith &
Coates, 1998 ; Fig. 14.1A, E, H in Smith & Coates, 2001).
Most importantly, those on the branchial arches were
spatially and temporally ordered as denticle whorls, features
both the oro-nasal and dermal denticle assemblages lacked,
leading Smith & Coates (2001) to propose that the key as-
pects of dentition patterning were present in pharyngeal
denticle whorls. As such, they reversed the classic scenario
and suggested an early origin of patterning of teeth from an
Zerina Johanson and Moya M. Smith
inductive endoderm (see the position of pharyngal denticle
whorls in Fig. 3B, ph.d) with co-option of this genetic
regulation for tooth sets at the margins of the mouth (Fig. 3).
Jollie (1968) had attempted to explain the homologies and
evolution of the visceral skeleton (=‘ splanchnoskeleton ’),
mainly that of the cartilaginous gill supports in jawed and
jawless gnathostomes by presenting a hypothesis of the
functional evolution of the mouth and pharynx. In this, he
proposed that the expanded mouth and posterior migration
of the mandibular arch to join the hyoid arch for jaw sup-
port brought dermal denticles into the oral cavity, and that
these became enlarged to function as teeth. In this way he
included dermal bones and ‘ teeth ’ in his theory of evolution
of jaw supports (Fig. 3), dependent upon the assumption that
a lining of ectoderm covered the stomatodeum (early mouth
cavity) up to the opening of the oro-pharynx at its caudal
end. This was the site where the mandibular arch joined the
hyoid, representing the boundary between stomatodeal ecto-
derm and endoderm (Fig. 3A, B). Given these consider-
ations, the assumption was made that the pattern for tooth
development spread antero-posteriorly from ectoderm to
endoderm, in conjunction with mandibular arch formation
and posterior migration. The scenario envisaged teeth ex-
tending posteriorly into the oro-pharynx to ‘ hold and sub-
due increasingly larger and more active prey ’ (Jollie, 1968,
p. 95). The position of the hypophyseal canal is, in embry-
ology, a marker for the ectoderm-endoderm boundary, as
noted above. Development of dermal elements beyond the
back of the mouth, within the pharyngeal region, was also
not considered, essentially because none were known in
jawless fish, until those of Loganellia scotica were described
(van der Brugghen & Janvier, 1993). The developmental
derivation of ‘ membrane bones ’ on the palate was also not
mentioned (e.g. the parasphenoid), nor their assignation as
dermal bones challenged.
The most recent molecular and developmental data pro-
vide important examples of the participation of endoderm in
patterning skeletal elements of the splanchnoskeleton,
specifically, the hyoid and pharyngeal arches, as well as the
facial region. Using data from the chick, Ruhin et al. (2003,
p. 239) concluded that the ventral foregut endoderm ‘exerts
a regionalised patterning activity on the cephalic neural
crest to build up the primary facial and visceral skeleton in
jaws and neck ’. David et al. (2002, p. 4457) noted that data
obtained from the zebrafish showed that ‘ the endoderm
provides differential cues along the antero-posterior axis to
control ventral head skeleton development ’ (cartilage bars of
the pharyngeal arches). The patterning role of endoderm is
corroborated by earlier findings that the positional infor-
mation giving polarity to each pharyngeal pouch is estab-
lished in the endoderm of the embryo even after neural crest
migration into that region is experimentally prevented
(Veitch et al., 1999). This information was deduced from the
expression pattern of Bmp4, Fgf8 and Pax9 in the endoderm,
remaining the same both with and without neural crest cells
and suggested to be a putative inherited chordate pattern for
the serial arrangement of branchial arches.
Couly et al. (2002, p. 1072) investigated the contribution
of foregut endoderm to patterning of the dermal bones of
the face and noted that ‘ proximodistal and anteroposterior
Origin and evolution of gnathostome dentitions
polarity of the skeleton is dictated by the endoderm’. Also,
‘ in strong contrast to the foregut endoderm, neither the
ectoderm, nor the mesoderm display patterning properties
that lead to skeletogenesis of the facial bones’. Similar pos-
itional information could organise the pattern of pharyngeal
denticles, teeth and membrane bone of the splanchno-
cranium, but needs to be established experimentally in fish
(see Huysseune et al., 2002 for a review of endodermal par-
ticipation in odontogenesis in fish). In zebrafish mutants, the
initial iterative pattern in the pharyngeal region is depen-
dent on endodermal signalling, and is also required to make
the separate cartilages in the branchial arches (Piotrowski &
Nüsslein-Volhard, 2000). As Couly et al. (2002) have also
shown, these polarities are determined in the foregut endo-
derm well before the branchial pouches are formed. They
also showed that presumptive first arch endoderm will elicit
Pitx1 expression in the neural crest cells, a gene normally
activated in skeletogenesis of the teeth and jaws. Pitx2 is a
marker gene exclusively expressed in odontogenic epi-
thelium in the mouse, through the early stages of initiation,
position of tooth loci, and cytodifferentiation for morpho-
genesis (Mucchielli et al., 1997). In our observations of the
structural patterns in pharyngeal denticles we emphasise
that structures under putative control of the endoderm, such
as branchial whorls of Loganellia scotica and the pharyngeal
denticles on the placoderm postbranchial lamina, show a
distinct pattern from those of the skin. Another distinctive
feature is that they demonstrate a quite different addition or
replacement pattern relative to the external skin denticles.
Dermal denticles can also be ordered into linear patterns
(Purnell, 2001 ; Donoghue, 2002 ; Young, 2003; Section
II.1), but none compare to the spatiotemporal regulation of
patterns for tooth sets (Smith, 2003).
(2 ) Tooth retention and tooth addition
Our developmental model refines the consensus views,
based on the precise definition of teeth as single odontodes
(Reif, 1982 ; Sire & Huysseune, 2003) but emphasises that
they are component parts of a regulated and patterned
dentition. In the general model for development and growth
of the dentition, tooth sets have either replacement
mechanisms built into them, or teeth are retained and new
tooth addition is regulated to extend the tooth rows. The
way these are patterned is unique for each crown-group
gnathostome taxon, teeth being initiated within a specific
pattern (Smith, 2003). Ørvig (1973, p. 135) conceptually
considered the homology between dermal denticles, oral
denticles and teeth as paramount and conceived of teeth as
‘ superficial odontodes which had secondarily assumed a
submerged position ’. An explanation of ‘especially small
teeth ’ on the margins of teleostome (=Acanthodii+
Osteichthyes, Fig. 1) jaws was that they ‘continued to form
as superficial odontodes ’ (Ørvig, 1973, p. 135, i.e.
Eusthenopteron foordi Whiteaves, 1881). He envisaged the
phylogenetic sequence as starting from an ‘oral dermal
skeleton of superficial odontodes ’ in which super-
impositional growth was suppressed, then later changed to
‘ periodic addition at the margins – of the same generation ’.
New teeth, added only at one end of statodont tooth rows,
27
are an example of this type of odontode growth and as we
have proposed these evolved from denticle sets within the
pharynx (Section III.2) from which genetic regulation was
co-opted for sequential tooth addition.
With the classic concept as a basis, Ørvig (1973) at-
tempted to interpret growth and tooth replacement in fossil
forms, as part of a comparison of dentitions of acanthodians
with those of early actinopterygians and also of brachy-
thoracid arthrodires. In this he accepted that tooth replace-
ment did not occur in the dentition of brachythoracid
arthrodires and acanthodians, because they were of the
‘stephanodont’ type (statodont as in Section II.2, each tooth
fused to the bone and not exchangeable). By comparison
both taxa add teeth during growth, although from opposite
directions in the jaw (Long, 1986 ; Smith, 2003), to what he
termed the ‘ dermal jaw-elements ’ (gnathalia in placoderms)
and contribute to the biting surface by further wear-resistant
tissue growth into the supporting bone. Ørvig (1973) also
concluded that these differences precluded acanthodian and
placoderm dentitions evolving into the tooth-replacing
dentitions of osteichthyans, i.e. there are fundamental dif-
ferences among these groups, as recently proposed by Smith
(2003). To illustrate the growth process, Ørvig (1973)
examined a graded size series of gnathalia in the arthrodire
Plourdosteus canadensis (Woodward, 1892) and importantly
stated that they carried ‘ real teeth ’ (Fig. 12). Later, he gave
a more complete account of the structure and growth in
arthrodire gnathalia in which he discussed whether or not
periodic growth could actively occur on such abraded,
highly polished attrition facets of the biting areas (tusks and
cutting blades) of the jaws (Ørvig, 1980a). In both works he
published an elegant series of diagrams to show how growth
in concentric bands increased the dental field area with
each new tooth, to add to the tissues of the gnathal bones
(Fig. 12).
Ørvig (1977) had made a clear distinction between der-
mal denticles (including oro-pharyngeal denticles) and teeth
in his review of their histology and development, reserving
the term odontode for the former but not for teeth. Teeth
were distinguished as those structures developing in ‘sub-
merged positions ’ in precise locations on the dermal bones
of the mouth and pharynx and functioning in the appre-
hension, or processing of food, as is the case for arthrodire
placoderms. Conversely, Reif (1982) later proposed that
‘odontode ’ referred to all dentine units including teeth,
comparable as building units and including the ‘bone of
attachment ’. This consolidated the views of Schaeffer (1977)
who had proposed that ‘odontodes ’ were single modifiable
morphogenetic units in both the dermal skeleton and the
dentition, but emphasised the inclusion of the bone of at-
tachment, as did Smith & Hall (1993). Reif (1982) proposed
distinguishing teeth from other odontodes by a develop-
mental concept, one effectively based on that of the chondri-
chthyan dentition. Namely, that the mode of formation
for successional teeth was different from all other odontodes,
as only they develop on a dental lamina, equivalent to
Ørvig’s (1973) ‘ submerged position ’. This has become the
commonly accepted definition for vertebrate teeth, now
listed as one of four synapomorphies of crown-gnathostomes
and notably excluding placoderms (Goujet, 2001). Ørvig
28
(1973) also discussed the presence of a dental lamina and its
variance in all groups of jawed vertebrates as a continuous,
or discontinuous, permanent or non-permanent structure
for the provision of successional, replacement and same
generation teeth, terms later emphasised by Reif (1982; also
Sire & Huysseune, 1998). Exceptionally, Sire (2001) and
Sire & Huysseune (2003) have described denticles in the skin
of living teleosts as ‘extraoral teeth ’. They discount the lack
of a dental lamina and base their identification on lack of
phylogenetic continuity of these denticles with ‘ ancestral
odontodes ’, such that these external denticles are indepen-
dently derived only in certain groups of actinopterygians.
Reif (1982) reviewed the evolution of dentitions and
concluded that gnathostome-type teeth (characteristic of the
crown-group) had not evolved in placoderms because they
showed no evidence of teeth forming from a dental lamina.
The evidence Reif depended on for determining whether
teeth developed in this way in fossils was the presence of
tooth whorls, either at the symphyseal region, or along the
jaw, as fused tooth sets (see Smith, 2003). He considered
these as homologous with each tooth set in extant chondri-
chthyans, and to indicate a succession of individual teeth
produced from a dental lamina, in a comparable way to
those of tooth families in sharks (see Fig. 14.5 in Smith &
Coates, 2001). Tooth whorls were present in acanthodians
but notably absent from placoderms. However, Ørvig
(1973, p. 145) had previously noted a resemblance in growth
and tooth addition between acanthodian jaw elements and
the ‘ teeth ’ on the gnathalia of brachythoracid arthrodires,
and to those of tooth whorls in fossil sharks. Nevertheless,
Reif (1982) later dismissed this evidence for tooth addition in
placoderms because the tissues were known to be quite dif-
ferent from those of crown-gnathostome teeth, enamel or
enameloid absent and with semidentine (unipolar cell bodies
enclosed in the tissue, see Section IV.3).
Despite the different developmental model for the evol-
utionary origin of teeth from the one proposed herein, the
observations of Ørvig (1980 a, his Figs. 1–21) are very rel-
evant. He identified potential sites of new tooth addition in
smaller (assumed younger), unworn specimens and illus-
trated rows of teeth in several positions on all the gnathal
bones. For example, the supragnathal (upper jaw) of
Coccosteus cuspidatus Miller 1841 ex Agassiz ms, illustrated by
Ørvig (1973, his plate 17.3 ; Miles & Westoll, 1968) pos-
sessed both adsymphysial and lateral rows of teeth. Ørvig
considered that single teeth on each of the rows occupied a
peripheral ‘dental field ’ because of their association with
growth bands on the surface of the bone, successive growth
bands increasing the gnathal bone area and adding a new
tooth. These grew by areal addition of fields of new denticles
(Reif, 1982 ; Karatajute-Talimaa, 1998), and in this respect
tooth addition to the placoderm dental field was compar-
able. Because of these similarities to denticle fields, Ørvig
(1973) did not describe placoderm teeth as developing on a
dental lamina in the manner characteristic of all other jawed
vertebrates, hence the prevailing view that teeth are not
present in placoderms. Still, the real significance of Ørvig’s
(1973, p. 144, 1980a) views can be summarised by his ob-
servations of ‘ the successive addition of new teeth in one
direction … in alignment with already existing ones’ and
Zerina Johanson and Moya M. Smith
‘ the synchronous formation in consecutive stages of growth
of new teeth’. However, rather than depicting these data in
terms of denticle field theories, we have justified a develop-
mental interpretation of a discontinuous dental lamina lo-
cated at the base of each ‘ last added ’ tooth in the tooth row.
In the Placodermi this is interpreted as another manifes-
tation of the ‘ tooth whorl ’ concept (Smith & Johanson,
2003a, b). As outlined in a previous section (Section II.3), this
concept includes tooth primordia forming sequentially and
linked to the functional teeth (Reif, 1982), i.e. odontogenic
ability confined to specific loci in the mouth related to the
existing tooth rows. These primordia can be considered ex-
amples of qualitative changes in shared gene expression
patterns by control of gene transcription, either positive or
negative (see Minelli, 2003). Genes are either switched on or
off, for tooth positions alternating with tooth incompetent
regions, as a prepattern for tooth set spacing (see Streelman
et al., 2003 for recent model). Each one of these sites would
relate to new tooth development as explained by clonal
models of tooth programs, with each new tooth patterned
and regulated relative to previous teeth in the group, or row,
in a taxon-specific pattern (Smith, 2003). With regards
to the coccosteomorph arthrodires (Section III.1a ; Fig. 4),
Ørvig (1973, p. 140) noted that ‘it should be made fully
clear that the gnathalia in coccosteids carry real teeth ’.
Ørvig (1980 a, p. 157) also noted that ‘the number and
relative position of these dental fields in several forms agree
closely with each other ’, suggesting homology with other
arthrodiran taxa.
Two important additional points concern how these teeth
possess different patterns of addition, replacement and
growth, relative to the dermal tubercles (fields of denticles)
on the plates of the placoderm head and trunkshield and
their histology (by comparison to teeth in crown-group
gnathostomes). The first is that our observations indicate
that placoderm teeth are never added superficially or by
superimposition, as are all denticles. Two, teeth are not shed
individually but are retained (statodont dentition), and
dental tissues grow from each tooth site deep into the bone
to compensate for wear. For example, the main tusk on the
biting edge is formed from an ingrowing vertical column of
dentinous tissue (pleromic dentine, see Section IV.4), and
presumed to derive from the small teeth of the earlier stage
(Fig. 12, tk). Posterior and medial, or lateral to the cutting
edges, individual teeth remain in rows, but these were
described as being made of semidentine (Fig. 15 A–D, s.d),
the accepted characteristic placoderm tissue for dermal
tubercles (Figs. 15 E, F, 16 D–F ; Ørvig, 1980 a). Resolution
of the type of dentine present in newly formed and older
teeth, and the ingrowing tissue of the gnathal tusks, has
provided crucial data in the debate on the origin of teeth in
placoderms and is discussed below (Section IV.3).
( 3) Tissue growth in teeth and denticles
As we have observed (Smith & Johanson, 2003 a, b), when-
ever we have examined sections cut exactly through the
toothed part of the gnathal bone in arthrodires, the principal
central tissue component is regular, straight tubular dentine
as found typically in all other crown-gnathostome teeth
Origin and evolution of gnathostome dentitions
A C D Figs. 24–28. Ørvig, 1980 a). It is, however, noteworthy that
b.e gr.z s.d
t1 o.c
d.t
s.d
B
t4
bo
cr.d
E F
tu3
s.d
tu2
bo
tu1
Fig. 15. Diagrams to compare arrangement of tissue types in
gnathal bones and dermal tubercles in arthrodires. (A)
Plourdosteus livonicus (Eastman) (Fig. 5A in Ørvig, 1973) section
through the adsymphyseal tooth row below the biting edge
(b.e) ; growth zones of the bone (gr. z) coincide with each tooth
in the row, these show the vascular nature of the teeth (t1–4),
each made of semidentine (s.d) as seen in the higher magnifi-
cations shown in B and C. (B, C) Holonema westolli Miles, 1971
(Ørvig, 1980 b). Sections through the pipe-ridge on the medial
side of the infragnathal show the outer layer of semidentine
(unipolar odontocyte cells, o.c) over bone (bo). (D) Actinolepis
tuberculata Agassiz, 1844 (Fig. 10B in Gross, 1957) vertical sec-
tion through a medial spinelet on the dermal spinal plate with
quite regular tubular dentine (d.t), note each group of tubules
emerging from vascular canals in the bone, and few cell lacu-
nae. (E, F) Phlyctaenius acadicus (Whiteaves, 1881 ; Fig. 9B, E in
Gross, 1957) vertical sections through dermal tubercles with a
special coronal layer of unipolar cells (cr.d) and others dispersed
below this (s.d), over bone (bo). In F dermal tubercles are
superimposed from successive growth stages (tu1, tu2, tu3).
(Fig. 17). This is a key observation to question the suggestion
of similarity, even homology with dermal tubercles, although
they also can independently form orthodentine as in the
spinelets of the pectoral spinal plate (see below, Denison,
1978 b). The direction and arrangement of the dentine
tubules (tracks of the formative cell processes of odontoblasts)
reveal centripetal growth as the cells migrate within a cen-
tral pulp cavity in the process of forming the dentine tissue of
the tooth. The tooth tissue differs from semidentine (dentine
with enclosed cell body spaces) present in most, but not all,
placoderm dermal tubercles (Figs. 15E, F, 16). These ob-
servations of the exceptionally well preserved Gogo fossils,
such as those of Compagopiscis croucheri (Fig. 17), are crucial,
therefore, because they conflict with those reporting semi-
dentine tissue constituting the gnathal biting edges in
placoderms such as Plourdosteus livonicus (Fig. 15 A; and see
29
Ørvig (his Figs. 65, 66. 1980a) also recorded a different tis-
sue in the apparently edentate gnathal tissue of Pholidosteus
bidorsatus von Koenen, 1883 and described it as ‘compact
hard tissue without cells and possibly with tubules ’. The
discussion herein is important because despite the poor
preservation and the comments that ‘ these tubules …
probably result from collagen fibrils in the living state ’,
Ørvig (1980a, p. 154) does conclude that this is tooth den-
tine. He compares it with the lateral dental field corre-
sponding to those of the lateral tooth rows in Coccosteus
cuspidatus and Dinichthys herzeri Newberry, 1868. None of this
information has been assimilated into the accepted body of
knowledge concerning histology of the placoderm dentition,
no doubt because of the complexity of Ørvig’s (1980 a) dis-
cussion. The statement that ‘ Since the hard tissue does not
contain spaces for enclosed cells … it is clearly not semi-
dentine as in Plourdosteus ’ and may be some sort of pleromin,
compounds the confusion. Another rare reference (Bryant,
1934) is to a tissue containing the ‘ same fine radiating
tubules’ from a section of the symphysial denticle in the
infragnathal of the arthrodire Dinomylostoma buffaloensis
Hussakof & Bryant, 1919.
Statements regarding absence of teeth in the placoderm
dentition resulted in part from this evidence of semidentine
in the gnathal edges, being present in many types of dermal
tubercles of the dermal armour, and distinctive for placo-
derms (Ørvig, 1967). However, another important aspect
concerns the growth of the dentine when comparing teeth
with external dermal tubercles (Young et al., 2001). The
latter never show invasive growth of the pleromic tissue type
as in jawless vertebrates (psammosteid heterostracans,
Ørvig, 1967) and semidentine of the tubercles is frequently
interspersed between layers of bone, as several generations
of tubercles are added in layers by superimposition (Fig.
15F). However, pleromic dentine is a widespread vertebrate
phenomenon (see review by Smith & Sansom, 2000) where
the migratory cells of the dentine continue to produce den-
tine by invasive growth into all the soft tissue spaces of each
jaw bone, mostly of a harder, more mineralised type
(Section IV.4).
It seems that the repertoire of dentine types in both the
dermal and splanchnic skeletons is extensive (Figs. 15–18),
with remarkable variability of dentine tissues within placo-
derms to include larger dermal tubercles that may exhibit
quite regular tubular dentine, resembling orthodentine.
Denison (1978 b) selected several examples where the den-
tine of the dermal tubercles was more like regular dentine
(tubules without cell body spaces in the tissue). The ‘ taller
tubercles of the rhenanid Ohioaspis, the inner part of the
teeth of Pachyosteus, and especially the marginal spinelets on
the spinal plates of Actinolepis ’ all exhibit regions of tubular
dentine (Fig. 15 D; Denison, 1978 b, p. 15). Gross (1957, his
Figs. 10, 12–15 ; Fig. 15D) illustrated regular dentine in the
spinelet of Actinolepis tuberculata Agassiz, 1844 and in the
tooth plates of the ptyctodonts Rhynchodus major Eastman,
1898, Rhynchodus sp. and Ptyctodus sp. (Fig. 18 A, B). Denison
(1978 b) regarded this tubular dentine infilling the bone
trabeculae in the gnathal bones of ptyctodonts as ‘ true
dentine ’ (see Fig. 18 D–F), but Ørvig (1980 b, his Figs. 1–6)
30 Zerina Johanson and Moya M. Smith

Fig. 16. (A–F) Tubercles as dermal ornament, with histology of dentine types shown in vertical sections. (A) Typical shapes in a field
on the dermal armour of the acanthothoracid Romundina stellina Ørvig, 1975, Prince of Wales Island, Canada, GSC loc. 8234. (B, C)
Romundina sp., section through one stellate tubercle showing a cellular form of dentine in the body of the tubercle, above spongy
bone : in the higher magnification (C) the outer layer is penetrated by parallel tubules normal to the surface and few elongated cell
body spaces (lacunae), together they comprise what is known as semidentine (odontocytic dentine, with a distinct tubular mantle
layer and inner cellular layer). (D, E) An arthrodiran dermal tubercle Sedowichthys terrae-boreae (Bystrow, 1957 ; section number VNKT
388, personal collection V. Karatajute-Talimaa) example of semidentine with two very distinct zones to the semidentine ; a mantle
layer of parallel tubules extending from a row of cell body spaces, below this many unipolar cells in groups and dispersed within the
inner dentine (classic semidentine). This distinctive outer layer is also shown in Fig. 15 (cr.d) as the special coronal layer of Gross
(1957), the cell bodies (odontocytes) are aligned at the junction of mantle with inner semidentine (arrows). (F) Incisoscutum ritchiei
Dennis & Miles, 1981, BMNH locality 31, Gogo, Western Australia, arthrodiran dermal tubercle with small layer of semidentine
over cellular, spongy bone. Abbreviations as in Fig. 15. BMNH, Natural History Museum, London. GSC, Geological Survey of
Canada, Ottawa.

in his later paper, as in the earlier one (Ørvig, 1973) did not. not be orthodentine. It is significant, however, that Gross
Rather he considered it a specialised dentine of the pleromic (1957) considered this outer layer to be dentine (Fig. 15 A, B).
type formed by infilling an external bony hard layer and One example of a tubercle of Phlyctaenius acadicus
from its topographic position (inside bone, see Fig. 18 C) could (Whiteaves, 1881) was selected by Denison (1978b, his Fig. 9)
Origin and evolution of gnathostome dentitions 31

Fig. 17. (A–C) Compagopiscis croucheri Gardiner & Miles, 1994, WAM 94.12.2, right posterior supragnathal, vertical sections through
one tooth on the posterior row (arrow in C) to show the regular tubular dentine with fine terminal branches at the surface (A). The
higher magnification field is from the tooth in (B) where the entire cone of dentine is infilling a surface layer of atubular tissue. (A, B)
Photomicrographs taken in Nomarsky differential interference contrast optics.

as one ‘with orthosemidentine superficially and trabecular
semidentine centrally ’ (Fig. 15 E), as illustrated by Gross
(his Fig. 9 in Gross, 1957). These terms may only add to
confusion when attempting to compare teeth of placo-
derms with those of crown group gnathostomes, and little is
advanced by subdivision of regions in a tooth with different
terms for each, other than the accepted topographic ones of
mantle (outer) and circumpulpal (inner). This is best illus-
trated by the histology of dermal tubercles in Phlyctaenius
acadicus (Fig. 15E, F) where the outer mantle layer (semi-
dentine, or coronal dentine of Gross, 1957) is distinct from
the inner semidentine. Burrow & Turner (1999) provide an
extensive discussion of all the previous terminologies of
placoderm tubercular dentine and attempt to create five
distinctive categories, but these are still complex and con-
fusing. They also use two names for outer and inner dentine,
ortho-semidentine and meso-semidentine, whereas in reality
all the dentine is formed without leaving a distinct pulp
cavity, as the cells of the dental papilla become embedded in
the calcified product, hence all the tissue is semidentine in
this inclusive sense.
It remains true that the occurrence of orthodentine,
dentine with tubules and no enclosed cell bodies, is very rare
in the dermal skeleton of placoderms and should not be re-
garded as evidence for the origin of teeth from these dermal
tubercles (Burrow, 2003 ; Smith & Johanson, 2003 a, b ;
Young, 2003). We have to assume a widespread develop-
mental plasticity in the dermal armour of early vertebrates
(Smith & Sansom, 2000) and create simple classifications
that reflect this, such as acellular tubular dentine and cellu-
lar odontocytic dentine. By comparison with dentinogenesis
of modern derived dentine types in shark teeth, a develop-
mental interpretation was suggested for placoderm tuber-
cular dentine (Smith & Sansom, 2000). In this description,
two different cell types, by phenotypic expression from the
progenitor cells of the dental papilla, produce the outer and
the inner dentine. Both cell types become included in the
mineralised product, odontocytic dentine, so it is not an
exclusively tubular dentine, but the cells are unipolar as
defined for semidentine (Figs. 15 B, C, E, F, 16 D–F). They
may participate in its further maintenance, as coronal
odontocytes [ortho-semidentine of Denison (1978b) and
Burrow & Turner (1999)] and inner (pulpal) odontocytes
[trabecular semi-dentine (Denison, 1978 b) and meso-semi-
dentine (Burrow & Turner, 1999)] exemplified exactly by
Phlyctaenius acadicus (Figs. 15E ; Fig. 9A in Gross, 1957) and
Sedowichthyes terrae-boreae (Fig. 16 D, E).
As Denison (1978 a, p. 15) commented ‘ true dentine
is best developed among placoderms in the gnathals of
Ptyctodontida’. Although Ørvig (1980 b, his Figs. 1–6)
32
A C F tub
b.e
pl
D
d.t B
pl pl
o.c
b.e
G
pl
td
E b.e
Fig. 18. (A–G) Diagrams of pleromic, tubular dentine in
toothplates (gnathalia) of ptyctodonts. (A) Ptyctodus sp. (Fig. 15 in
Gross, 1957) section through biting edge (b.e) shows an outer
shell of dentine (d.t) infilled by trabecular dentine (td) and
pleromic dentine (pleromin, pl). (B) Higher power of mantle
dentine layer from outer edge with tubules linked to vascular
spaces. (C) Opposing edges of upper and lower tooth plates of
Ctenurella gladbachensis Ørvig (Fig. 3 in Ørvig, 1980 b), with
harder, translucent pleromin infilling the outer shell of dentine.
(D–F) C. gladbachensis (Figs. 26, 28 in Ørvig, 1980b) increasing
magnification diagrams of the tubular dentine (tub) and pos-
ition of the formative cells (o.c) with cell processes ; direction of
growth of pleromin shown by white arrows. (G) Left toothplates
in situ attached by quadrate–articular jaw joint of perichondral
bone Rhynchodus tetradon Jaekel, 1903 (Fig. 1 in Ørvig, 1980b).
Black arrows show fields of higher magnification drawings.
discusses pleromin in ptyctodonts, and illustrated sections
through these tooth plates showing true dentine-like tissue
(Fig. 18 C–F), he debated as to whether or not this was the
same as the superficial tissue in a tooth and was reluctant to
call it orthodentine. Ørvig did emphasise the acellularity of
pleromin and noted the ‘total lack of enclosed scleroblast
spaces’, while unicellular scleroblasts are diagnostic of
semidentine. Lack of semidentine in ptyctodont tooth plates
was used by Ørvig (1980b, p. 326) to separate ptyctodonts
from arthrodires, where he had shown the presence of
semidentine alone, and concluded that ‘ ptyctodonts are not
really placoderms in the strict sense ’.
It seems that we can conclude that there is considerable
plasticity in the occurrence of semidentine in placoderms,
additionally, many tubercles are made of bone alone, or
only a superficial layer of irregular semidentine (Fig. 16 F).
However, in certain groups regular dentine would appear to
be associated with the growth of the dentition in ptyctodonts
as graphically illustrated by Ørvig (1980b ; our Fig. 18 F),
where cell bodies are outside the forming dentine, and in
certain arthrodires as we have shown there is regular den-
tine (Fig. 17). New teeth, those added individually, have
not been recognised in ptyctodonts, and instead the dentine
is produced by continuous invasive growth, as illustrated
in figure 18, which we believe is a derived condition and
one showing great disparity in jawed vertebrates. In the
arthrodires, by comparison, the dentition grows and dentine
is added through the addition of new teeth to existing
rows (Figs. 11 E, G–I, 17 C), and only with wear of these
does pleromic semidentine appear (see section IV.4). The
Zerina Johanson and Moya M. Smith
situation where new teeth are added to an established tooth
row, each made of orthodentine, is most comparable to the
condition in other jawed vertebrates (Section II.3).
( 4) Adaptive growth and tissue remodelling
A mechanism for maintenance of biting surfaces and adap-
tation to wear becomes a pre-requisite for survival with any
statodont type dentition. The massive jaws of the 9 m long
Devonian placoderm Dunkelosteus terrelli Lehman, 1956, and
those of taxa such as Gorgonicthys Claypole, 1892, are con-
spicuous for their enormous tusks and blade-like cutting
edges, with diminutive teeth located in a row at the posterior
end (Fig. 6). These and other pachyosteomorph arthrodires
were described in Section III.1.a. These cutting blades and
the toothplates of the Ptyctodontida provide two divergent
examples of hypermineralised, ingrowing dentine of the
pleromic type and ones in which the growth has been de-
scribed and well illustrated by Ørvig (1973, 1980 b). Also, the
tissue growth in the cutting blades and tusks of the toothed
gnathals in Plourdosteus canadensis and P. livonicus has been the
main focus of Ørvig’s (1973, 1980 a) papers and this tissue
growth is discussed herein (see Figs. 12, 15A). As may be
obvious, ‘the upper and lower gnathalia work against each
other like a pair of shears – often sharp edged and polished
by wear ’ (Ørvig, 1973, p. 140, 1980a, p. 51). A type of
invasive growth with tissue remodelling in the interior
compensates for the tissue lost by abrasion at the functional
surface of the gnathal bones (Figs. 12, 18). The upper
gnathal plates have two rows of teeth in Coccosteus cuspidatus
and Plourdosteus canadensis (Fig. 12 A, B). Each tooth is made of
a richly vascular core (Fig. 15 A) and the interior is composed
of bone (osteosemidentine), and the outer of pallial semi-
dentine [in the terms of Ørvig (1973) ; see Section IV.3].
The contrast is made between these teeth with continuous
ingrowing dentine and the semidentine tubercles of the
dermal armour. Columns of semidentine beneath the main
tusk of the biting edge are described as forming by complete
fusion of the consecutive, semidentine teeth (see Fig. 12).
Increase in size of the whole gnathal bone is by addition of
trabecular bone at the soft tissue surface, converted into
dense, compact bone by osteone formation (these are illus-
trated in Fig. 19 D, E). Within this skeletal trabecular bony
framework, thought to provide the growth sites for the
pleromic dentine tissue, the primordial tissue of the semi-
dentine columns arises (Ørvig, 1973). The direction of
growth in this type of infilling dentine is clear from the
direction of the tubules (Fig. 18 A, C–E, white arrows,
Fig. 19A–C, p.d).
We can add significant new data from images taken with
a scanning electron microscope and from sections through
these regions of growth (Figs. 11, 19) in different gnathal
plates. Although previously unrecorded, these show bio-
logical activity of resorption of the tissues and redeposition
of layers of both dentine and bone, in active remodelling
growth. New teeth are added to the new bone (Fig.
11A, E–I) and layers of smooth, white tissue coat all these
surfaces (probably dentine), each interpreted as equivalent
to a growth layer (arrows, Fig. 11 C, as shown by Fig. 5
in Ørvig, 1980a). On the bone surfaces below the teeth
Origin and evolution of gnathostome dentitions 33

Fig. 19. Remodelling of gnathal tissues by pervasive growth of dentine into spongy bone (A–C) compared with infilling by osteonal
bone (D, E). (A–C) Vertical sections of Antineosteus lehmani Lelièvre, 1984, MNHN MCD207, infragnathal through both ridge (ri) and
denticle (dent) tissue (see figure 9 for topography and structure) made of compact, dense atubular dentine. Similar dentine fills in the
vascular spaces of the bone below, as shown in higher magnifications (B) where the lighter coloured dentine fills in the vascular
spaces pervasively (arrows) and in C (pl) deep to the biting surface. The light coloured dentine (pl) is relatively unstained by the
process of fossilisation and contrasts with the crystalline diagenetic material (**) filling the remaining soft tissue spaces in the bone.
(D, E) Dunkleosteus sp. MNHN MCD 17, vertical sections through the gnathal bone, below the cutting edge resorption has taken
place along the medial surface (arrows, compare with cutting edge resorption in other species shown in Fig. 11 D, E, G). Deep inside
the bone remodelling has occurred with new osteones (os) highlighted by a diagenetic change to their biological structure.
Abbreviations as defined previously.

osteoclast resorption pits are seen, either minimal in extent
(Fig. 11A, B), or very extensive as at the medial side of
the infragnathal of Incisoscutum ritchiei (Fig. 11 E–G). This
effectively removes much of the bone and infilling dentine
(arrows in Fig. 11 D), but is later replaced by new bone layers
and especially is accompanied by selective deposition on the
lateral side of the bone. This is most clearly seen where the
cutting surface has a new layer of bone and dentine is added
to a previous resorption surface, with a clear disjunction of
the tissue structure (arrows in Fig. 11G). Comparative sec-
tions through other pachyosteomorph arthrodires show a
similar disjunction, and a resorbing edge (arrows, Fig. 19D).
34
Inside the gnathal bone remodelling occurs as new osteones
fill in the vascular spaces (Fig. 19 D, E, os).
The histology of dentine growth in Antineosteus lehmani
Lelièvre, 1984 reveals how extensive the ingrowing dentine
becomes (Fig. 19 A–C) from the denticles and ridge tissue
(for the topography of these structures see Fig. 9). The
lighter, less stained and harder dentine is without tubules
and can be seen to infill all the available spaces of the vas-
cular canals (Fig. 19 C, p.d) similar to that of bone in form-
ing osteones in compact bone (Fig. 19 D, E, os). In this way,
hard wear resistant tissue is created, by forming within the
denticles or teeth at the surface, this creates extensive, all
pervasive growth of the pleromic dentine (compare with Fig.
18). This is an impressive adaptation to non-replacement of
teeth as a character of placoderm dentitions and we are only
beginning to understand in which taxa it is a dominant
feature. This development and growth of dentine is perfectly
possible to observe in well-preserved material, especially in
those which retain the record of all growth stages until lost
by wear.
(5 ) The placoderm oral cavity
Reif (1982) denied that placoderms possessed a dentition
generated within a dental lamina but he also discussed the
concept of ‘ tooth families ’ (as occur within a tooth whorl),
including the functional tooth and all its successors.
However, Smith & Coates (2001) revised this and referred
to a ‘ tooth family ’ as a ‘generative set ’, and Smith (2003)
suggested that this concept can accommodate the den-
tition of arthrodires. Thus, description of the actinolepid,
pachyosteomorph, ‘ primitive brachythoracid ’ and coccos-
teomorph tooth rows (see Fig. 4), considers the ‘functional
tooth ’ to be the active biting edge in these taxa, to which the
successor teeth are continually added at one end only, as in a
generative set. This can be determined at least in growing
gnathal bones, to which new teeth are being added (Figs.
6–9, 10 A–D). In some taxa, such as the pachyosteomorph
arthrodire Heintzichthys gouldii, this tooth addition appears to
end at some point in ontogeny. Reif (1982) placed great
importance on the presence of tooth spirals (whorls) in other
basal groups of jawed vertebrates (e.g. chondrichthyans and
acanthodians), in which teeth of successive generations are
fused to a common bone of attachment (the only form of
bone in chondrichthyans). By comparison, ‘bone of attach-
ment ’ has also been observed surrounding the bases of the
new teeth added to arthrodiran tooth rows (Fig. 9), event-
ually being merged or incorporated into the new gnathal
bone as the teeth became part of the functional biting sur-
face. In Heintzichthys gouldii (Fig. 8 A), this bone of attachment
underlies and joins all teeth in the row, equivalent to the
common bone of attachment described by Reif (1982).
These common features suggest that the tooth rows ob-
served in certain arthrodire taxa are comparable, both
morphologically and in terms of their development, to tooth
whorls or tooth sets. This development must involve a dental
primordium (‘ primordial tissue ’, or tooth placode of epi-
thelium and competent mesenchyme) to create each new
tooth at the end of the tooth row, similar to that illustrated
deep within the dental lamina by Reif (1982, his Fig. 3).
Zerina Johanson and Moya M. Smith
However, the arrangement of the tooth rows in arthrodires
suggests their primordia are located at widely spaced and
restricted positions on the gnathal plates. In these
arthrodires, the concept of a discontinuous, rather than
continuous, dental lamina is more appropriate, in which the
tooth-producing tissues are restricted to certain points along
the dentate bones (Reif, 1982). A comparable condition is
shown by lungfish with a tooth-plated dentition, in which
teeth are added to specific loci at regulated positions, de-
termined by the sites of tooth primordia, along the margin of
the plate (Smith, 1985, 1988, 2003).
Denticles can be associated with the tooth row in ar-
throdire taxa such as the pachyosteomorph Gymnotrachelus
hydei and the ‘ primitive brachythoracids ’ Antineosteus lehmani
and the new ‘buchanosteid ’ of Young et al. (2001). In these
taxa, distinct tooth rows are present in which new teeth are
added to regulated positions at the end of the row.
Accompanying denticles, most notably in Antineosteus lehmani,
appear to be incorporated into biting surfaces, a process
involving resorption and redeposition of dental material. In
the phlyctaeniid arthrodires (e.g. Dicksonosteus sp.) and the
Phyllolepida rows can sometimes be visually reconstructed
amongst the denticle patches, but spaced tooth rows, re-
duced in number, are not present. We refer to the units
added to these dentitions as oral denticles, reserving the
term ‘ teeth ’ for dentitions conforming to the developmental
model outlined in Section III.1. New denticles form outside
the functional biting surface as do new teeth in our devel-
opmental model with some element of patterning, but ad-
dition is not as strictly regulated as that of new teeth. All
denticles are retained and resorption does not appear to
occur. The genetic networks involved in producing regu-
lated dentitions may not be refined in the Phyllolepida, but
this morphology, with regulation of denticle addition only to
the margins of the preexisting plate or denticle area may
represent an early or precursor developmental state in the
placoderm phylogeny. In some individuals, this regulation
(compare Fig. 10 F, G and 10E), is not fixed or consistent
within the groups and precise tooth families, or sets, cannot
be recognised.
With regard to the crucial morphology of the placoderm
dentition at the base of the clade, the groups Acanthothor-
aci, Rhenanida and Antiarchi are of prime importance.
However, very little information is available from the
Acanthothoraci, while the Rhenanida and the Antiarchi are
characterised by the incorporation of external dermal
headshield units into the dentition, whether the suborbital
(antiarchs) or tesserae (Jagorina pandora). The rhenanids show
notable variation in the morphology of the dentition ; be-
sides Nefudina qalibahensis and Jagorina pandora, the infra-
gnathals of some specimens of Gemuendina stuertzi appear to
include ordered rows of denticles, comparable to the
phlyctaeniid arthrodire Dicksonosteus and the Phyllolepida.
Denticles cover the paired anterior supragnathals of the
acanthothoracid Romundina sp. and differ essentially in their
arrangement from those on the headshield, especially
the ventral aspect of the median rostral plate (Smith &
Johanson, 2003a). This is just one variant of widely diverse
morphologies unrelated to establishing teeth in a regulated
pattern in more derived placoderm taxa, which we contend
Origin and evolution of gnathostome dentitions
happens within the Arthrodira (Smith & Johanson,
2003 a, b).
By evaluating the character states of dentitions in out-
group taxa, character polarity can be determined. Because
the Placodermi is resolved as the plesiomorphic sister taxon
to all others in the cladogram of jawed vertebrates (Fig. 1),
jawless vertebrates such as the Osteostraci and the
Heterostraci are pertinent to this discussion (dentitions of
the jawless group Anaspida have not been described). The
Osteostraci has been resolved as the sister group to the clade
of jawed vertebrates (Young, 1986; Goujet, 2001 ; Janvier,
2001), and in this major clade any type of dentition is very
poorly known. The oral cavity is described in only a few
taxa, for example, in Tremataspis mammillata Patten, 1931, the
oral cavity is very small and covered in small denticles, re-
stricted to just beyond the cavity opening (Fig. 17 A in
Janvier, 1985). Nevertheless, it is significant that these den-
ticles do not merge morphologically into external headshield
structures. This condition is more similar to the dentition of
the acanthothoracid Romundina sp., and indeed most other
placoderms and all other jawed vertebrates (Smith &
Coates, 1998, 2000, 2001) and may represent the plesio-
morphic condition for the jawed vertebrates. However, as
noted above (Section II.1), Purnell (2001) demonstrated that
denticles at the oral margin of the Heterostraci merged, or
intergraded morphologically, into dentine ridges on the ex-
ternal surface. These are comparable to the dentition of
antiarchs and certain rhenanids, which also incorporate
external dermal elements into the oral cavity for use as
feeding structures, with the ornament on the external sur-
face of these continuous with ornament on the external
headshield surface (Fig. 10 I, J). Perhaps the structural ar-
rangement in these groups rather than that of the
Osteostraci and Acanthothoraci represents the plesio-
morphic condition for jawed vertebrates. This state involves
a limited incursion of dermal denticles to the oral margin,
compared to the classic view of a more extensive cover of
denticles in the oral cavity. A later step in this scenario was
proposed to be a more extensive distribution leading to
denticles covering the pharyngeal cavity, the entire popu-
lation derived from the ectodermal genetic programmes.
However, the condition in the Antiarchi and Rhenanida
should not be viewed as a ‘first step ’ in this classic evol-
utionary scenario. In these groups, dermal elements rep-
resent the functional dentition, but clearly do not satisfy the
morphological requirements for the identification of teeth,
as applied by us to the Arthrodira. Denticles in the phar-
yngeal region of the Antiarchi and Rhenanida are organised
into rows of polarised denticles (Johanson & Smith, 2003;
Section III.2.b), but patterning is lacking from the dermal
elements in the oral cavity (as well as in the Heterostraci).
The pharyngeal denticles are well separated from the oral
dermal elements, with no morphological continuity within
the oro-pharyngeal region. This evidence suggests that pat-
terning mechanisms are associated with the pharyngeal
denticles, and that this is prior to utilisation of these mech-
anisms in the oral cavity, conforming with the paradigm
that co-option is from the pharyngeal region to the oral
cavity (Smith & Coates, 1998, 2000, 2001), rather than
vice versa.
35
These characters of the oral and pharyngeal cavities need
to be evaluated in the context of a phylogenetic analysis
including both jawless and jawed vertebrates, similar to
those of Janvier (1996b), Donoghue et al. (2000) and
Donoghue & Smith (2001). Notably, these analyses did not
include ‘ teeth ’ as a separate character, while Donoghue &
Smith (2001) coded ‘ denticles in pharynx ’ as absent for
placoderms. It will be vital to incorporate our new ob-
servations into more stringent and robust phylogenies, es-
pecially as only a very limited sampling of the placoderm
taxa was utilised. Current phylogenies are also problematic
in separating Loganellia scotica (Thelodonti) from the clade of
jawed vertebrates, not only by other thelodonts (Donoghue
and Smith, 2001), but also by the Osteostraci (Smith &
Coates, 1998), the latter lacking any indication of denticles
on their gill arches. This results in homoplasy and character
convergence on these current phylogenies (Fig. 1), particu-
larly with respect to the Conodonta, phylogenetically the
first taxon to possess a patterned dentition in the oro-phar-
yngeal cavity.
The group Placodermi is striking among jawed ver-
tebrates in the variety of dentitions represented, and as we
have argued, includes teeth which are morphologically and
developmentally the same as those in other jawed ver-
tebrates (Smith & Johanson, 2003 a, b). Such teeth occur only
in derived placoderm taxa, within the Arthrodira, leading to
two possible conclusions regarding dental evolution in the
jawed vertebrates. The first is that current phylogenies are
incorrect (e.g. Figs. 1, 2, 4), and that arthrodires possessing
teeth are more closely related to other jawed vertebrates (i.e.
the Placodermi is a paraphyletic group, see Section II.4).
The second conclusion is that these phylogenies are correct,
and that teeth evolved independently within the Placodermi
and are non-homologous with respect to the teeth of other
jawed vertebrates (Smith & Johanson, 2003 a, b). Essentially,
teeth may have arisen several times in the gnathostome lin-
eage (Section I.4) thus provoking a need to re-evaluate
phylogenetic analyses of the placoderms and jawed ver-
tebrates.
(6 ) The placoderm pharyngeal cavity
Recent phylogenetic analyses consider pharyngeal denticu-
lation to be absent for the Placodermi (Donoghue & Smith,
2001). A consequence of this proposed absence is that jaw-
less fish such as Loganellia scotica, with their patterned phar-
yngeal denticle whorls, share a primary homology with
jawed vertebrates that placoderms lack (i.e. an initial hy-
pothesis of homology, sensu de Pinna, 1991). It is significant,
as described here, that the gill arches of certain placoderm
taxa possess bases of bony gill rakers ; their regular, spaced
pattern indicative of some controlling regulatory mechan-
ism, while all placoderm taxa possess patterned denticles on
the postbranchial lamina. Although this denticulated surface
is situated at the rear of the pharyngeal cavity, posterior to
and not supported by the gill arches (Fig. 3 D), we propose
that the denticulation pattern is generated inside the phar-
yngeal cavity, despite it being described as part of the
trunkshield. This is relevant to the suggestion that there is
separate regulation of pharyngeal developmental pattern
36
from that of the dermal exoskeleton (odontodes). The con-
cept of separate modular developmental units for teeth,
cartilages and bones (Smith & Hall, 1993), including all as-
sociated mineralised elements of the splanchnocranium,
whether cartilage, bone, denticles, or gill rakers (Smith &
Coates, 1998, 2000, 2001) is also relevant. Evidence from
the zebrafish indicates that teeth (present only on the 5th
branchial arch) are present in ‘flathead ’ mutants while all
other gill arch elements (cartilage and bone) are lacking
(Graveson, Smith & Hall, 1997; Smith & Coates, 2001),
supporting their modular nature. In other words, denticles
need not be associated with pharyngeal cartilages but can be
associated with other bones such as those internally pos-
itioned as part of the trunkshield. It also suggests that these
pharyngeal teeth were strongly conserved in the gnatho-
stome body plan as a persistent phenotype.
A variety of actinopterygian taxa also possess rows of
denticles posterior to the gill arches and associated with the
cleithrum and clavicle (summarised by Patterson, 1977).
The most intriguing of these are the chondrostean Polyodon
spathula Walbaum, 1792 (Grande & Bemis, 1991, 1996) and
the neopterygian Amia calva Linnaeus, 1766 (Liem & Woods,
1973; Jarvik, 1980; Grande & Bemis, 1998). In Amia calva,
serrated appendages (homologous to the clavicle) carry long
rows of denticles supported on triangular protrusions along
a bony ridge (Liem & Woods, 1973). Ontogenetically, the
thin bone of the clavicle forms prior to the denticle rows
(Liem & Woods, 1973), such that their development at this
stage is independent. These denticle rows differ from the
ornament on the external surface of the cleithrum in
smaller individuals, where the denticles for the most part
occur in a simple row along the bony ridges and the
triangular, or pyramidal protrusions, are rarer (Liem &
Woods, 1973). In larger (older) individuals, the number of
denticle-covered triangular protrusions increases on the ex-
ternal cleithrum surface and the ornament here is similar to
that preserved on the clavicle (Jarvik, 1980 ; personal ob-
servations ZJ on MCZ 25088, Museum of Comparative
Zoology, Harvard). Although on the external surface, this
part of the cleithrum is still covered by the operculum (M.
Coates, personal communication, 2002), and could be con-
sidered to occur within the boundaries of the pharyngeal
cavity.
Scales, differing from those located on the body, are
located on the external surface of the cleithrum in the fossil
taxon Peipiaosteus pani [Acipenseriformes (Fig. 8 in Grande &
Bemis, 1996)]. Morphologically unique scales are also as-
sociated with the pectoral girdle of the extant paddlefish
Polyodon spathula [Acipenseriformes (Fig. 23 in Grande &
Bemis, 1991)], and appear to occur under and on the
pharyngeal side of an opercular flap, comparable to the
condition in Amia calva. In Polyodon spathula, the arrangement
of scales follows the curvature of the edge of the opercular
flap and the bones of the pectoral girdle. Perhaps most sig-
nificantly, the presence of these post-gill arch denticles in
living actinopterygians implies that the contribution of an
endodermal layer to the development of these denticles as-
sociated with the pharyngeal cavity can ultimately be tested.
This would provide evidence pertinent to the fossil groups
such as the Placodermi and the patterned denticles on the
Zerina Johanson and Moya M. Smith
postbranchial lamina, based on an assumption that genetic
regulation at the pattern level is conserved within these
jawed vertebrate groups.
Among sarcopterygians, comparable denticles are rarer,
although they do occur in the phylogenetically basal fossil
taxon Psarolepis (Zhu et al., 1999). Here the postbranchial
lamina is covered in rows of triangular denticles, differing in
morphology and arrangement relative to those of the ex-
ternal surface of the cleithrum (M. Zhu, personal com-
munication 2002). On the lamina of Youngolepis praecursor
Chang & Yu, 1981, the ornamentation is composed of bony
ridges. These ridges are oriented differently relative to the
external surface of the cleithrum (and parallel to the medial
margin of the postbranchial lamina) and are straighter and
more evenly spaced. By comparison, the ridges on the ex-
ternal surface appear to anastomose throughout their length
(Chang, 1991, her plate 6).
The presence of ridges, scales or denticles associated with
the pectoral girdle either on the postbranchial lamina or
underneath the opercular flap would seem to be a feature
occurring only in placoderm and osteichthyan fishes (Zhu &
Schultze, 2001). In both instances, these elements form
within the boundaries of the pharyngeal cavity. Comparably
located elements appear to be absent in chondrichthyans
and in acanthodians. Considering that pharyngeal denticles,
or scales, can occur in crown-group gnathostomes posterior
to the gill arches and in association with the pectoral girdle,
Nelson’s (1970 b) observations for chondrichthyans are sig-
nificant. He illustrated the pharyngeal denticles for a variety
of taxa, with the distribution of these forming a particularly
sharp boundary just posterior to the last pharyngeal arch ;
no denticles occurred posterior to this boundary (Figs. 1, 2, 5
in Nelson, 1970b). This suggests that the mechanisms in-
volved in producing and patterning denticles in chondri-
chthyans were not present posterior to this last arch.
Again, the location of the boundary between endoderm
and ectoderm relative to the position of these pharyngeal
denticles could be tested in extant chondrichthyans. In
acanthodians dermal plates are associated only with the
ventral parts of the pectoral girdle (Denison, 1978 a).
Additionally, the scapula of Diplacanthus crassimus is divided
into what are described as a posterior flange and a post-
branchial lamina (Denison, 1978 b), although denticles are
clearly absent from the latter.
The influence of pharyngeal patterning on the oral cavity
may be demonstrated by the brachythoracid arthrodire
Holonema westolli (Fig. 8O–Q). In general, the trend on the
placoderm postbranchial lamina is for denticles near the
growth origin of the lamina to be smaller, increasing in size
as the animal itself grows (Johanson & Smith, 2003).
However, in Holonema westolli, the denticles are large in this
original position and maintain this size across the post-
branchial lamina (Fig. 8P, Q). Notably, the dentition of
Holonema westolli is unusual, made up of vertical ‘pipes ’
of semidentine (Fig. 15 B, C ; Miles, 1971, his Fig. 15 O).
The size of these pipes is equal across the dentition of the
gnathal plate and does not increase during growth. Thus,
this may represent an instance where the pharyngeal
pattern regulating size of structures is co-opted to the
dentition.
Origin and evolution of gnathostome dentitions
V. CONCLUSIONS
(1) Placoderms possess a diverse range of dental
morphologies. Despite this, teeth can be distinguished from
denticles and identified within the Placodermi, contrary to
recent opinion (Young et al., 2001 ; Zhu & Schultze, 2001;
Donoghue & Sansom, 2002 ; Burrow, 2003 ; Young, 2003).
This information fills an important gap in data for stem
gnathostomes at the base of the clade of jawed vertebrates
(Fig. 1). Amongst the Arthrodira, and more specifically the
actinolepid and eubrachythoracid arthrodires, new teeth
form at the ends of tooth rows, at predetermined positions,
during growth within the statodont dentition. Both the
mode of tooth addition, restricted to the ends of rows, and
tooth non-replacement, are comparable to that of the stato-
dont dentitions of certain acanthodians, chondrichthyans
and osteichthyans. From current consensus placoderm
phylogenies we conclude that teeth in the Arthrodira are
convergently acquired and not homologous (i.e. lack of
phylogenetic continuity) with teeth of the crown-group
gnathostomes.
(2) An alternative to the conclusion above is that phylo-
genies of the Placodermi and jawed vertebrates are incor-
rect. Incorporation of these revised characters on the
distribution of denticles and teeth as characters in a data
matrix will test different tree topologies. These new analyses
may resolve whether or not the Placodermi are para-
phyletic, and whether the arthrodires are more closely re-
lated to members of the crown-group Gnathostomata ; if
supported, there would be few grounds for suggesting that
teeth were derived independently within the Placodermi.
(3) For each placoderm clade the postbranchial lamina of
the anterior trunkshield supports organised denticles dis-
tinctly different in their arrangement and morphology from
those of the dermal ornament. Phylogenetically, these pat-
terned pharyngeal denticles appear prior to teeth, providing
an example of an early manifestation of a regulatory gene
network for the organised tooth rows in the placoderm
dentition which may be a synapomorphy of jawed ver-
tebrates (Fig. 1).
(4) The placoderm groups Antiarchi and Rhenanida
incorporate external dermal elements into their feeding
apparatus, but we stress that these are not teeth, neither in
their morphology, nor their development, nor as part of a
patterned dentition. A similar incursion of external dermal
denticles into the oral cavity was described for the
Heterostraci (Purnell, 2001), where organisation or pattern
to the heterostracan oral denticles is not apparent, apart
from a similar outward orientation.
(5) Notably, external dermal denticles are restricted to
the anterior parts of the antiarch and rhenanid oral cavity.
Thus, the classically accepted evolutionary scenario, with
posterior migration from the external skin into oral and
then pharyngeal regions can be questioned as there is no
morphological continuity with the patterned denticles
covering the postbranchial lamina in these basal groups.
Additionally, denticles covering the placoderm para-
sphenoid differ morphologically from those externally.
Therefore, we suggest that external skin denticles never
reached the buccohypophyseal opening, currently the only
37
accepted position of the boundary between the earlier em-
bryonic endodermal and ectodermal layers and could never
have provided ectodermal patterning information to regu-
late tooth sets. Considering these observations in their
totality we suggest they provide compelling evidence that
external denticles evolved independently from oro-pharyn-
geal ones, the latter produced by the endoderm.
(6) A developmental model can be proposed from these
phylogenetic data, the basis of which is endoderm in the
provision of pattern control. The essentially different pat-
terns of the two skeletal systems have their evolutionary
origins in the skeletogenic inductive ability of the endoderm
in relation to regulatory control of the splanchnocranium,
compared with that of the ectoderm for the dermal skeleton.
The latest data from experimental developmental genetics
show that endoderm is essential and required for the early
regulation of pattern in amniotes (chick) and the zebrafish,
for the development of the pharyngeal arches (cartilage and
bone of the splanchnoskeleton) and also for facial bones. We
suggest this regulatory mechanism from endoderm can also
be utilised for denticles and teeth as part of the splanchno-
cranial skeleton. Stem-group gnathostomes, resolved phylo-
genetically, should be used as markers for early incidence of
developmental states from which hypotheses of evolutionary
process can be made.
(7) Homologies can be divided into those related to pro-
cess and to pattern (Minelli, 2003). The process of odontode
(tooth, scale, denticle) formation extends to the base of the
total-group Gnathostomata (Fig. 1, character 1: Donoghue
& Sansom, 2002). A node more crownward in the phylo-
geny, independence of internal and external odontodes
occurs, as illustrated by the Conodonta and other jawless
vertebrates (Fig. 1, characters 2, 3). This independence in-
cludes the patterning mechanisms involved, with separate
and distinct regulatory systems existing for the internal and
external odontodes. The presence of a genetic network in-
volved in patterning odontodes in the pharyngeal cavity is
independently derived in the Conodonta, Loganellia scotica
and jawed vertebrates (Fig. 1, character 6). The patterning
mechanisms may involve a unique genetic toolkit in the
Conodonta, to regulate the different arrangement of
conodont elements, characteristically mediolateral occlusion,
rather than dorsovental. However, the independent origins
of these mechanisms in Loganellia scotica and jawed ver-
tebrates are more problematic. Current phylogenies indicate
that Loganellia scotica is a derived thelodont, resulting in the
resolution shown in Fig. 1 (Donoghue & Smith, 2001).
Importantly, these phylogenies did not code pharyngeal
denticles as present in placoderms, nor did they include any
characters describing their internal patterning. The number
of characters supporting the various nodes in the Thelodonti
is low (Donoghue & Smith, 2001) and the addition of new
characters may overturn these hypotheses. Alternatively,
we could consider that the regulatory networks responsible
for patterning pharyngeal denticles are resolved as a
synapomorphy at the node incorporating the Thelodonti
and jawed vertebrates, with absence of expression in basal
thelodonts and the Osteostraci. Notably, absence of ex-
pression of this gene network (absence of teeth in a regulated
dentition) does occur in basal placoderm groups such as the
38
Acanthothoraci and Antiarchi and may support absence of
expression in other stem-gnathostome groups. However,
following current phylogenies of the jawed vertebrates and
the Placodermi, the origin of the structures (teeth) patterned
by these gene networks in the oral cavity (Fig. 1, character 5;
Smith, 2003) does occur separately within placoderms
and potentially independently in each of the crown-group
gnathostomes.
(8) We find no evidence, phylogenetic or morphological
to support classic theories of evolution in which teeth evolve
from the internal migration of external dermal elements into
the mouth.
VI. ACKNOWLEDGEMENTS
First and foremost we would like to thank Drs John Long (Western
Australian Museum, Perth), Daniel Goujet and Herve Lelièvre
(Museum national d’Histoire naturelle) for providing extremely
generous access to their specimens, including unpublished
material. Funding from National Geographic and Australian
Geographic has supported John Long’s fieldwork. We would like to
thank all three of these researchers for their help and for in-
numerable discussions on placoderm dentitions and phylogenies.
We also thank Gavin Young (ANU, Canberra) for access to his
unpublished material. Reviews provided by Philip Donoghue
(University of Bristol) and Mike Coates (University of Chicago)
helped us to clarify many of our arguments and we are grateful to
them for subsequent discussion. Drs Gloria Arratia (Museum für
Naturkunde, Berlin), Mike Williams, Gary Jackson (Cleveland
Museum of Natural History) and Alex Ritchie (Australian
Museum) allowed us to photograph specimens for this work, in-
cluding undescribed phyllolepids. Drs Long, Goujet, Lelièvre,
Arratia, Williams, Jackson and Joe Hannibal (Cleveland Museum
of Natural History) are also thanked for their very kind hospitality
during study visits. Dr Michael Wuttke very helpfully provided
several new casts of specimens of Gemuendina stuertzi for study. We
also thank Dr Kate Trinjastic for discussions, access to material
under her care and for generous hospitality. We would like to
thank Sue Lindsay (Australian Museum) for taking our S. E.M.
photomicrographs. M. M. S. thanks the Royal Society for providing
study grants for work at the Australian Museum (2001, 2003), and
the Australian Museum for a Visiting Fellowship (2003). Z. J. is
funded by an Australian Research Council Senior Fellowship.
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Permission to reproduce the following figures is gratefully acknowledged : Fig. 4: Blackwell Publishing :
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Society 47, 99–120; Fig. 5 : Royal Society of Edinburgh from Transactions of the Royal Society of Edinburgh,
volume 67 (1968), pp. 373–476 ; Fig. 10E, Elga Mark-Kurik, Institute of Geology, Tallinn Technical
University, Tallinn ; Fig. 10F, G, Alex Ritchie, Australian Museum, Sydney ; Fig. 10H, Daniel Goujet,
Museum national d’Histoire naturelle, Paris ; Fig. 10I, Gavin Young, Australian National University,
Canberra ; Fig. 10 J : The Palaeontological Association, UK (http://www.palass.org/). Young, G. C.
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ostracoderms, placoderms and fossil elasmobranchs. 3. Structure and growth of gnathalia of certain
arthrodires. Zoologica Scripta 9, 141–159 ; Fig. 15 A, E. Schweizerbart Science Publishers, Stuttgart (http://
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