Teeth in placoderms
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Supplementary Online Material -1079623
Early fossil jawed vertebrates provide evidence for separate evolutionary
origins of teeth
Materials and methods
Our observations are based on placoderms from the Upper Devonian Gogo Formation,
Western Australia, in a unit renowned for the excellent structural and histological
preservation of unaltered three-dimensional material (S1-S3). Using these fossils it has
been possible to compare the upper and lower jaw dentitions (gnathalia) of several
placoderm taxa, all within the Arthrodira (Eubrachythoracida) (Fig. 1B). The gnathalia
were prepared with natural biological surfaces of the dentition exposed and examined by
optical and scanning electron microscopy. This approach allowed us to identify new teeth
relative to old ones in functional rows (Fig. 2, S1), and hence determine both the polarity
of tooth addition to statodont rows (non-replaced sets of teeth) in placoderm dentitions
and the degree of wear. Some Gogo material was also selected and cut vertically through
new teeth and worn, biting surfaces (Fig. 2, S2). This provided histological observations
using Nomarsky optics to compare with sections through placoderm dermal tubercles.
Thus, the type of tissue in each situation and its growth could be compared and
contrasted. Institute Abbreviations: AMF: Australian Museum, Sydney; FM-P: Field
Museum, Chicago; NHM-P: Natural History Museum, London; WAM: Western
Australian Museum, Perth.
Supporting text
Although ordered rows of ‘true teeth’ along gnathal edges in one arthrodire taxon
(Plourdosteus) have been previously described (S4), these were claimed to form patterns
in the adult dentition arranged in dental ‘fields’ as if they were superficially generated,
comparable with those of external skin denticles. Our observations indicate that the
dentition is formed from patterned linear rows of teeth in which new ones are added to
deep loci at the ends of these rows only (Fig. 2B - F: Fig. S1A - E, arrows), and are
inferred to develop here from tooth primordia below the oral epithelium, in tissues
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comparable to a dental lamina. Each tooth is added directly in line with the previous tooth
in the row but out of the functional plane. Each is fused via its ‘bone of attachment’
(tooth related bone) to the new bone surfaces on all three gnathal bones (Fig. 2A),
anterior and posterior supragnathals (upper jaws) (Fig. 2C, D; Fig. S1 C-E, S2A)
infragnathal (lower jaws) (Fig. 2B, E, F; Fig. S1A, B). Whereas the majority of examples
show teeth added to cutting edges in a sectorial type (Fig. 2A-F; Fig. S1A, B, S2A),
another of a durophagous, or crushing dentition also shows new tooth addition well away
from the functional surface, on the inner aspect (Fig. S1C-E). In this morphology there
are multiple rows of closely packed teeth lateral to the functional surface, to each of
which new teeth are added from below the bone surface by a soft tissue structure (Fig.
S1D, E). Here, three new teeth are forming sequentially, one to each of the three tooth
rows, associated with newly forming bone developing at the base of the supragnathal
(Fig. S1E).
Figure S1. A-E, tooth addition to the upper and lower dental (gnathal) plates of different
morphological types of arthrodiran taxa (Placodermi). Arrows indicate newest tooth
added to row. A, Aethaspis sp. (Actinolepida), FM-P4117, left infragnathal, internal
view, showing at least three separate tooth rows. B, Incisoscutum ritchiei
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(Eubrachythoracida), AMF95644, SEM of symphyseal tooth row on left infragnathal
(internal view). C-E, Bullerichthys fascidens(Eubrachythoracida), WAM74.2.59,
posterior supragnathal; C, ventrolateral surfaces, functional biting surface to the left; D,
dorsal (soft tissue) surface. E, closeup of soft tissue surface, showing new teeth added to
three tooth positions (loci, white arrows), the newest is the top one (in the photograph)
with a thin dentine shell and open pulp cavity. Double arrow indicates equivalent tooth
row in Fig. S1C, D.
In sections through the toothed part of the gnathal bone (Figs. 2H-I; S2 B, C) the
principal central tissue component is typical branching, tubular dentine as found in all
other gnathostome teeth. 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 central pulp cavity in the process of forming the tissue dentine of the
tooth. Therefore, contrary to previous accounts of the tissue constituting the gnathal
biting edges in placoderms (S4), these teeth are made of the same dentine as most
gnathostome teeth. The tooth tissue differs from that of most placoderm dermal tubercles,
which is described as semidentine (S5, S6), the characteristic dentine type found only in
placoderms (Fig. S2 D, E). Previously, the absence of dentine and presence of
semidentine in the placoderm dentition, along with lack of a pulp cavity, were used to
reject the presence of teeth in placoderms and to suggest derivation from the dermal
tubercles (S6).
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Figure S2. A, Compagopiscis croucheri WAM 94.12.2 (Arthrodira), right posterior
supragnathal with position of section (B, C) marked (white line) on the posterior tooth
row. B-E, histological sections through new tooth on upper gnathal bone and tuberculate,
placoderm dermal armor. B, C. croucheri vertical section through dentine of one tooth,
lateral to the pulp chamber, with boxed area to show field of (C). C, higher magnification
shows dentine tubules with sub-parallel and branched arrangement, tapering at the
surface, but without lacunae for cell bodies in the tissue. D, E vertical section through an
external dermal skin tubercle of the placoderm Romundina sp. (Acanthothoraci) showing
semidentine with unipolar lacunae (arrows) and tubules directed outwards, as cell bodies
(arrow) are contained within dentine rather than in pulp cavity.
Only one clade of placoderms possess teeth composed of regular dentine and
tooth rows developed in a regulated pattern comparable with those of other jawed
vertebrates (see main text), namely the derived placoderm group Arthrodira (S1, S2).
However, this pattern may be one that is distinctive for placoderms (S7). Although
observations here are confined to the arthrodire group Eubrachythoracida (Fig. 1B), tooth
addition in this placoderm-specific pattern is also present in the Actinolepida (Fig. S1A)
(S8, S9), representing a basal arthrodire taxon. In basal placoderms (Acanthothoraci,
Rhenanida, Antiarchi, Ptyctodontida) teeth as characterised for the Arthrodira are absent
(S10). Although in ptycotodonts there is a form of regular tubular dentine, it forms as an
ingrowth of dentine into the bone of the gnathalia (S11) and separate teeth do not appear
to precede this morphology (S11, S12).
Despite its apparent complexity at the patterning level, this way of adding new
teeth to the dentition in placoderms appears to have been acquired independently within
the jawed vertebrates. Mapping the character ‘teeth’ to the base of jawed vertebrates in
the cladogram, together with jaws (Fig. 1A), requires one additional step (loss in basal
placoderms then a second gain within arthrodires) when compared to independent
(convergent) origins of teeth, and so is less parsimonious. We propose that basal jawed
vertebrates are toothless and teeth, with specific patterning controls for tooth position and
timing of addition, evolved at least twice.
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Clues as to the molecular developmental mechanisms of these patterning controls
may be found in recent investigations on sequential development of both individual teeth
and in particular, cusp development in mammalian molars (S13-S15). In the molars, the
spatial-temporal pattern of expression uses the same ‘tool kit’ of genes for each cusp and
reveals a pre-pattern for cusp arrangement distinctive for each molar type (S13, 14).
Presumably a similar molecular pre-pattern could be predicted to occur, with the same
conserved multigene signal families to mediate the development of each new tooth within
the domains of a dental lamina. These other types of complex events, including tooth
position and timing of initiation along the jaw, can occur in all vertebrates. There is
repeated use of molecular signals at successive developmental stages in the mammalian
dentition (S15), as shared molecular ‘tool kits’ mediate sequential and reciprocal toothproducing epithelial-mesenchymal interactions.
Although we consider that toothed dentitions originated independently within
jawed vertebrates, the developmental programme underlying histogenesis of the unitary
tooth itself also underlies histogenesis of the skin and pharyngeal denticles, within the
concept of the developmental module, or odontogenic unit (S16, S17). As such, this
particular molecular ‘tool kit’ may be a deeply nested homology within the vertebrates,
also operating in all basal jawed vertebrates.
References
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S3. J. A. Long, Zool. J. Linn. Soc. 94, 233 (1988).
S4. T. Ørvig, Zool. Scrip. 9, 141 (1980).
S5. T. Ørvig, Phylogeny of tooth tissues: evolution of some calcified tissues in early
vertebrates, in Structural and chemical organization of teeth, A. E. W. Miles, Ed.
(Academic Press, New York, 1967), pp. 45-110.
S6. G. C. Young, H. Lelièvre, D. Goujet, J. Vert. Paleo. 21, 670 (2001).
S7. M. Meredith Smith Evol. Dev. (in press).
S8. R. H. Denison, Fieldiana: Geology 11, 461 (1958).
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S10.
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R. H. Denison. Placodermi, in Handbook of Paleoichthyology, H. –P. Schultze,
Ed. (Gustav Fischer Verlag, Stuttgart, 1978).
S11.
T. Ørvig, Zool. Scrip. 9, 219 (1980).
S12.
J. A. Long, Geodiversitas 19, 515 (1997).
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J. Jernvall, S. V. E. Keränen, I. Thesleff. Proc. Nat. Acad. Sci. 97, 14444 (2000).
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I. Salazar-Ciudad, J. Jernvall. Proc. Nat. Acad. Sci. 99, 8116 (2002).
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S. V. Keranen, P. Kettunen, T. Aberg, I. Thesleff, J. Jernvall. Dev. Genes Evol.
209, 495 (1999).
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M. Meredith Smith, B. K. Hall, Evol. Biol. 27, 387 (1993).
S17.
M. Meredith Smith, M. I. Coates, in Major Events in Early Vertebrate Evolution
(Systematics Association Special Volume Series 61), P. E. Ahlberg, Ed. (Taylor &
Francis, London, 2001), pp. 223-240.
Moya Meredith Smith
Craniofacial Development
Dental Institute KCl
Guy’s Campus
London Bridge, SE1 9RT, UK
Corresponding author: ž HYPERLINK mailto:Moya.smith@kcl.ac.uk
− Moya.smith@kcl.ac.uk
Tel: +44 207 955 4414
FAX: +44 207 955 2704
Zerina Johanson
Palaeontology
Australian Museum
6 College Street
Sydney, NSW, Australia 2010.
email: ž HYPERLINK mailto:zerinaj@austmus.gov.au − zerinaj@austmus.gov.au
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