Journal of
Applied Ichthyology
J. Appl. Ichthyol. 30 (2014), 636–642
© 2014 Blackwell Verlag GmbH
ISSN 0175–8659
Received: November 12, 2013
Accepted: February 2, 2014
doi: 10.1111/jai.12532
Review
Old, new and new-old concepts about the evolution of teeth
By P. E. Witten1, J.-Y. Sire2 and A. Huysseune1
1
Research Group ‘Evolutionary Developmental Biology’, Biology Department, Ghent University, Gent, Belgium; 2UMR 7138,
Universit
e Pierre et Marie Curie, Paris, France
Summary
The evolutionary origin of teeth from dermal denticles
(odontodes) that developed in the mouth cavity, designated
as outside-in hypothesis, has long been undisputed. The outside-in hypothesis is based on the conclusion that dermal
denticles and teeth fulfil the criteria of homology in an exemplary manner. Over the past 15 years, this hypothesis has
been challenged. Proponents of the alternative inside-out
hypothesis suggest that teeth did not evolve from dermal
denticles, that they are of endodermal origin (forming in conjunction with neural crest-derived mesenchyme) and that they
evolved several times independently in different lineages of
vertebrates. Key arguments for the inside-out hypothesis are
mineralized structures of conodonts that are accepted as
teeth, the exclusive acceptance of placoderm pharyngeal denticles as teeth, together with the rejection of the presence of
teeth in basal placoderms. We summarize the results of
recent studies that have been triggered by the fruitful discussion between the two conflicting hypotheses. New findings
support the traditional outside-in hypothesis: the mineralized
elements of conodonts are not teeth, and the oral cusps in
basal placoderms are true teeth. Furthermore, new developmental and molecular data clarify homology between teeth
and dermal denticles. Today a new synthesis is emerging
about the evolutionary origin of teeth from dermal denticles
and about the unity of the elements of the dermal skeleton.
cap. On the body surface they were transformed into
odontocomplexes, from which arose various types of scales
(Huysseune and Sire, 1998; Sire et al., 2009). In chondrichthyans, individual odontodes are still present as dermal
denticles (also called placoid scales) (Hall and Witten, 2007).
Development of teeth and dermal denticles requires interactions between the epithelium and the underlying mesenchyme
(see also Hall, 2014; in this volume). Also the developmental
pathways that produce these structures are highly conserved
(Miyake et al., 1999; Sharpe, 2001; Debiais-Thibaud et al.,
2011). The sequence of appearance of odontodes and teeth in
the fossil record and the shared characters that establish the
homology between teeth and odontodes are the basis for the
classical hypothesis, according to which teeth derive from
odontodes that developed in the oral cavity when the jaws
formed in early gnathostomes (Hertwig, 1874; Ørvig, 1967;
Reif, 1982; Smith and Hall, 1990). This view is also designated as the outside-in hypothesis (Blais et al., 2011).
Phrased in a more developmental way, teeth derive from
odontogenically competent ectoderm that expanded into the
mouth cavity and interacted with competent neural crestderived mesenchyme. This ectoderm could then have transferred its odontogenic competence to endoderm as suggested
by Huysseune et al. (2009, 2010) (Fig. 1). R€
ucklin et al.
(2011, 2012) endorse the idea that, ultimately, teeth and
other oral and pharyngeal denticles must be derived through
the extension of the odontogenic capacity of the external dermis to the internal dermis and endoderm.
The classical view about the origin and evolution of teeth
Teeth are highly conserved elements of the vertebrate skeleton. Notwithstanding some examples of derived tooth types
(see e.g. Huysseune and Sire, 1998; Davit-Beal et al., 2009;
Sire et al., 2009), teeth in all toothed vertebrates are made
from dentine and covered by a hypermineralized cap. Inside
they have a pulp cavity that is vascularized and innervated
(Sire and Huysseune, 2003). These principal characters of
teeth are shared with the basic units of the dermal skeleton,
the odontodes (De Beer, 1928; Ørvig, 1977; Reif, 1982; Smith
and Hall, 1990; Janvier, 1996; Huysseune and Sire, 1998).
Odontodes were mineralized elements of the dermal skeleton
that were present in the first, jawless, vertebrates (Donoghue
and Sansom, 2002). Odontodes are made of dentine surrounding a pulp cavity and covered by an hypermineralized
U.S. Copyright Clearance Centre Code Statement:
An alternative view on the evolution of teeth
The long-time undisputed outside-in hypothesis on the evolutionary origin of teeth has been challenged in a series of publications that suggested that (i) teeth evolved more than
once, and (ii) teeth evolved independent from odontodes in
the pharynx of ancient vertebrates and (iii) are thus of endodermal origin (Smith and Coates, 1998; Smith and Johanson,
2003; Fraser et al., 2009; Fraser and Smith, 2011). The conjecture that pharyngeal teeth could have evolved prior to oral
teeth and expanded into the mouth cavity led to a new
hypothesis, designated as the inside-out hypothesis (Fraser
and Smith, 2011) (Fig. 1). The inside-out hypothesis builds
on a number of postulates:
0175-8659/2014/3004–636$15.00/0
The evolution of teeth
637
which teeth (or structures interpreted as teeth) appear in
the fossil record, is taken as evidence that teeth evolved
multiple times in vertebrates (Smith, 2003).
Two conflicting hypotheses
Fig. 1. Schematic representation of the outside-in and the inside-out
hypothesis for the evolution of teeth. The outside-in hypothesis as
rephrased by Huysseune et al. (2009, 2010) postulates that ectodermderived odontodes invaded the mouth and the pharyngeal cavity, via
the mouth openings and via different branchial openings. Eventually,
ectoderm-derived odontogenic competence could have been transferred from ectoderm to endoderm (co-option). Intermediate stages
between dermal denticles and teeth in proximity to jaw margins further support the idea that tooth and dermal denticles are homologous. The inside-out hypothesis postulates the parallel evolution of
teeth and dermal denticles. According to this hypothesis, teeth
evolved in the endoderm-covered oropharyngeal cavity. The postulated parallel evolution of teeth in conodonts and in placoderms, as
well as the assumed lack of intermediate stages between dermal denticles and teeth have been quoted to support the inside-out hypothesis. Developmental data in extant vertebrates that show tooth
development in ectoderm-covered and in endoderm-covered locations
are differently interpreted by the proponents of the two conflicting
hypotheses. Both hypotheses accept co-option. Red arrows indicate
the postulated direction of tooth expansion in evolution. Blue represents ectoderm and ectoderm-derived skeletal structures, dermal denticles and teeth. Green represents endoderm as well as the proposed
endoderm-derived teeth. This cartoon was inspired by Huysseune
et al. (2009), and from figures published Fraser et al. (2010), and
Blais et al. (2011).
1 Conodonts are accepted as vertebrates and mineralized
conodont structures have been accepted as teeth (Donoghue and Sansom, 2002). These ‘teeth’ are believed to
be located inside a pharynx (Donoghue et al., 2000).
Consequently, conodont ‘teeth’ are assumed to be endoderm-derived. Since conodonts lack a dermal skeleton,
the first vertebrate tooth-like structures would have
evolved before odontodes (Johanson and Smith, 2005).
2 In Placodermi, the most basal clade of jawed vertebrates,
and also in Chondrichthyes, the arrangement of ectoderm-derived dermal denticles indicates the lack of a dental lamina. Following a definition of Reif (1982),
odontode-derived structures that develop without a dental
lamina are not accepted as teeth. Consequently, in placoderms, only pharyngeal, but not oral, denticles are
accepted as teeth. These teeth are again assumed to be of
endodermal origin (Smith and Coates, 1998; Smith, 2003;
Johanson and Smith, 2005).
3 If structures are homologous one would expect to find
transitory stages between these structures during development and/or in the fossil record. It is suggested that transitory stages between endoderm-derived teeth and
ectoderm-derived dermal denticles are lacking (Smith and
Coates, 1998; Johanson and Smith, 2005).
4 The assumed phylogenetic relationships between conodonts, placoderms and eugnathostomes (jawed vertebrates except placoderms), and the inferred sequence in
The inside–out hypothesis was never undisputed. Opponents
do not accept conodont mineralized structures as teeth,
refuse the idea about a multiple origin (convergent evolution)
of teeth, and emphasize the firmly established homology of
odontodes and teeth (Burrow, 2003; Sire and Huysseune,
2003; Reif, 2006; Huysseune et al., 2009). Clearly, an ongoing productive debate about the developmental and evolutionary origin of teeth has triggered several studies, all of
which challenge the above listed postulates of the inside-out
hypothesis and support the classical outside-in hypothesis
(Huysseune et al., 2009; Turner et al., 2010; Blais et al.,
2011; R€
ucklin et al., 2011, 2012; Murdock et al., 2013; Qu
et al., 2013). Thanks to this fruitful debate, a refined understanding of the evolution of dermal denticles and teeth is
emerging. We here summarize the results of the recent
studies.
Mineralized conodont elements are not teeth
Two papers published by a group of prominent palaeontologists in 2010 re-evaluated conodont characters and the phylogenetic position of conodonts (Blieck et al., 2010; Turner
et al., 2010). The authors conclude that conodonts are not
vertebrates, possibly not even chordates. Blieck et al. (2010)
emphasize the lack of fossil material that supports the popular reconstruction of conodont animals, eel-like vertebrates
with huge, unprotected eyes in front of a snout. Conodonts
are removed by these authors from the vertebrate tree
because of the extreme low level of cephalisation, the lack of
a dermal skeleton or any other vertebrate skeletal tissue such
as cartilage, and the lack of segmentally arranged paraxial
elements. The conodont trunk musculature is simple Vshaped and not W-shaped as it is the case for vertebrates.
Most important for the evolution of teeth, the conodont
mineralized structures contain a large-crystal, albid material
(also called white matter, an essentially opaque formless tissue, characterized by voids) that is neither dentine nor
enamel nor enameloid. Their growth is continuous, and they
could have functioned in a way similar to the feeding apparatus of some non-vertebrates, such as polychaete annelids
(Turner et al., 2010). The latter authors endorse the analysis
of Reif (2006) who emphasized that there is no way to
homologize odontodes and teeth with conodont elements on
the basis of fabric, of structure, of topological relationship,
of inferred developmental tissue relationship, of histogenetic
principles and of a morphogenetic program. Superficially,
conodont elements can resemble small fish teeth, but conodont elements can be morphologically indistinguishable from
serrated mineralized fossil annelid structures (Marshall et al.,
2013). Different from Turner et al. (2010) and Reif (2006),
Murdock et al. (2013) emphasize that there are structural
similarities between vertebrate odontodes and euconodont
638
mineralized elements. Still, the authors agree that euconodont elements are not teeth but an example of convergence.
Whether conodonts are vertebrates, chordates, or not even
chordates, is still a matter of controversy (Purnell et al.,
2013). Within the context of this review, it is important to
point out that those scientists that support the idea that euconodont animals are vertebrates, agree that mineralized
conodont elements are unrelated to dermal denticles or teeth.
Conodont elements are now regarded as feeding structures
analogous to structures encountered in vertebrates and nonvertebrates (Murdock et al., 2013). The removal of conodont
elements from the list of odontode/tooth-related structures
removes a cornerstone of the inside-out hypothesis.
Oral denticles of placoderms have tooth characters
In addition to mineralized conodont structures, the insideout hypothesis refers to tooth whorls located in the pharynx
of thelodonts (jawless vertebrates) as a second example that
teeth evolved ‘inside’, in an endoderm-lined setting, and were
subsequently co-opted to colonise the jaw margins ‘insideout’ (Smith and Coates, 1998). These oropharyngeal denticle
whorls are accepted as teeth based on the assumption that
their patterning suggests successional development and thus
development from a dental lamina. Huysseune et al. (2009,
2010) agreed with their identification as teeth, but at the
same time pointed out that their location is consistent with
an ectoderm-derived origin. Denticles covering the postbranchial lamina in placoderms likewise have been assigned a
‘tooth’ status based on their inferred ordered addition (Johanson and Smith, 2005). As is the case for thelodonts, this
location is an area where invagination of ectoderm could
have carried odontogenic competence deep into the body
(Huysseune et al., 2009, 2010). R€
ucklin et al. (2012) have
since demonstrated that the tooth-like structures on the postbranchial lamina of placoderms are merely focal developments of continuous sheets of spongy bone.
Denticles located in the skin and internal oral mucosa in
basal placoderms are considered by Smith and Johanson
(2003) to develop synchronously and thus without a dental
lamina, and are therefore not accepted as teeth. Smith and
Johanson (2003) furthermore identify ‘true teeth’ based on
their regulated addition in association with the gnathal bones
in advanced, but not in basal placoderms. This led them to
suggest that teeth are the result of convergent evolution. Burrow (2003) has disputed the denial of tooth-like structures on
the jaw bones in basal placoderms, showing staggered rows
of tubercles on the gnathals in basal placoderms, similar to
the structures in advanced placoderms, interpreted by Smith
and Johanson (2003) as teeth. A recent analysis of placoderm
gnathal ossifications with Synchrotron X-ray Tomographic
Microscopy (SRXTM) supports Burrow’s view (R€
ucklin
et al., 2012). The examination of a developmental series of a
placoderm (Compagopiscis croucheri, Arthrodira) clearly
shows oral tooth cusps that develop successionally (not synchronous). The cusps are composed of dentine, and have distinct pulp cavities. Pulp cavities are lined with centripetally
nested tissue layers permeated by radially arranged and polarized canaliculi, typical of dentine tubules. Such arrangement
P. E. Witten, J.-Y. Sire and A. Huysseune
and structure of oral cusps in placoderms clearly reveals correspondence with odontodes and teeth. R€
ucklin et al. (2012)
and Giles et al. (2013) conclude that the teeth that they identify in the earliest jawed vertebrates are homologous to the
teeth of crown gnathostomes and, as a consequence, that
teeth did not evolve convergently among extant and extinct
classes of early jawed vertebrates. The homology of teeth
and dermal denticles is also supported by a recent analysis of
developmental stages of fossil acanthodians with phase contrast X-ray Synchrotron microtomography (PPC-SRmCT).
This study also shows a dentition-like patterning of dermal
denticles (Qu et al., 2013). Confirming that the mechanism of
odontode (denticle) development corresponds to that of gnathostome teeth, Qu et al. (2013) further argue for the homology of teeth and dermal denticles and refute the idea that
oropharyngeal elements and external odontodes are fundamentally different. Indeed, the enormous diversity of dermal
denticles and tooth patterning in extinct and extant vertebrates (Huysseune and Sire, 1998; Sire and Huysseune, 2003;
Witten et al., 2005; Sire et al., 2009) invalidates arguments
about convergent evolution of teeth and dermal scales that
refer to different patterns. Moreover dermal scales and teeth
are developmental modules (Stock, 2001; Donoghue and
Sansom, 2002; Johanson et al., 2008). If these modules
acquire a new function as teeth inside the oral cavity, it is
safe to assume that their patterning changes together with
the new function.
The many shapes of the dental lamina
The dental lamina is a thickened band of epithelial tissue
that initiates tooth development by making contact with
competent mesenchyme. Subsequently, the epithelium differentiates into the outer and inner dental epithelium. The latter
provides ameloblasts that secrete enamel. The mesenchyme
provides odontoblasts that produce the dentine matrix (De
Beer, 1928; Huysseune and Sire, 1998; Tucker and Sharpe,
2004). In vertebrates with repeated tooth replacement the
dental lamina can be continuous or discontinuous, and permanent or non-permanent (Reif, 1982). For example, a discontinuous and non-permanent dental lamina can arise anew
from the outer dental epithelium of a more developed tooth
at the time it will be replaced (successional dental lamina,
Huysseune and Thesleff, 2004). Reif (2006) suggested that
development from a dental lamina distinguishes teeth from
other odontode-derived elements. Although the dental lamina
is not preserved in the fossil record, its presence or absence
(inferred from the pattern of candidate tooth structures)
plays an important role in the discussion if denticles in the
oropharyngeal cavity are accepted as teeth. For example, a
suggestion about the independent evolution of teeth in the
placoderm group Arthrodira recognizes structures located on
placoderm gnathal plates as teeth, also because their arrangement suggests the presence of a dental lamina (Smith and Johanson, 2003; Johanson and Smith, 2005). Conversely, the
tooth status of oral cusps in less derived placoderm groups is
not recognized since their arrangement does not indicate the
development from a dental lamina. The in-depth structural
analysis of oral cusps in Arthrodira by R€
ucklin et al. (2012)
The evolution of teeth
confirms their tooth status. These authors, however, point
out that, based on their structural criteria, the oral cups in
other placoderm groups can be recognized as teeth as well.
This, and data that indicate that Arthrodira are close relatives of chondrichthyans and osteichthyans, led these authors
to conclude that placoderm teeth did not evolve independently from gnathostome teeth. We like to emphasize that
living jawed vertebrates show a great diversity in epithelial
connectivity between predecessor and successor. In Atlantic
salmon, for example, functional teeth and replacement teeth
develop in such close apposition that a dental lamina cannot
be recognized as a distinct strand of epithelial tissue. Still,
replacement teeth develop from the outer dental epithelium
of the predecessor tooth (Huysseune et al., 2007; Huysseune
and Witten, 2008). The same situation is observed in the
basal bony fish Polypterus senegalus (De Clercq et al., 2014,
in this volume). Such an intimate connection between predecessor and replacement tooth could well explain the arrangement of oral denticles in placoderms.
Dermal denticles inside the oral cavity
There is little doubt that the developmental mechanisms that
produce dermal denticles and teeth are essentially identical
(Debiais-Thibaud et al., 2011). Correspondence between
teeth, dermal denticles and various scales is also established
for their structure, microstructure and cellular composition
(De Beer, 1928; Miyake et al., 1999; Sire and Huysseune,
2003). Also, mutation of ectodysplasin (EDA) or of its
receptor (EDAR) in zebrafish selectively affects skeletal elements evolutionarily derived from ectoderm: fin rays and
scales, as well as pharyngeal teeth (Harris et al., 2008; Harris, 2012). Obviously, there is little leeway for arguing
against the common descent of dermal denticles, scales and
teeth from the odontodes that were present on the body surface of early, jawless vertebrates. If, however, teeth in extant
vertebrates develop from endoderm, could that prove that
odontodes, dermal denticles and teeth are not homologous?
Darwin was convinced that embryonic development and larval stages show us, more or less completely, the condition of
the progenitor of the whole group in its adult state (Darwin,
1859, p. 345). Ever since, and despite vivid debates about
the extent of validity of this concept, scientists analyze development also to obtain insights into evolution (von Baer,
1828; Haeckel, 1866; Gould, 1977; Raff, 1996; Hall, 1998).
Likewise, ontogeny is also studied to elucidate the relationship between dermal denticles and teeth (Donoghue, 2002).
Teeth that develop deep inside the oral cavity and pharyngeal teeth are often assumed to be of endodermal origin
(Jackman et al., 2004; Fraser and Smith, 2011). For the
Mexican axolotl (Ambystoma mexicana) and for mice it has
been suggested that only teeth at the jaw margins derive
from ectodermal epithelium (Tucker and Sharpe, 2004;
Soukup et al., 2008; Ohazama et al., 2010). In mammalian
embryos, the epithelium located posterior to the buccopharyngeal membrane is viewed to be endoderm (see review by
Soukup et al., 2013). Teeth that develop posterior to the
buccopharyngeal membrane should thus be endodermderived. However, a recent study from the laboratory of A.
639
Tucker in London used endoderm labelling in a Sox17-2AiCre/Rosa26 reporter mouse. Their study revealed that endoderm has no contribution to tooth development at any stage
of development. In the mouse all teeth, including the last
molar, are entirely ectoderm-derived (Rothova et al., 2012).
Development is often conserved, but not always. Thus we
can not know for sure whether processes of tooth development in the axolotl or in the mouse are conserved or
derived. The mouse experiments by Rothova et al. (2012)
provide, however, precise identification of endoderm and
solve the question about the possible contribution of endoderm to mouse tooth development (Tucker and Sharpe,
2004). In carp, that have only pharyngeal teeth, ectoderm
penetrates inwards into the presumptive pharyngeal slits of
the embryos and covers the endoderm, as observed by
Edwards (1929). In fossil temnospondyl amphibians, pharyngeal teeth disappear together with the disappearance of the
gill openings (Schoch, 2002). These findings led Huysseune
et al. (2009, 2010) to suggest that during evolution tooth
development did depend on competent ectoderm invading
the oropharyngeal cavity via the mouth opening and via the
gill slits, or rather via ectoderm-endoderm contacts preceding
the formation of the slits. They coined the term ‘modified
outside-in’ for this hypothesis. Development evolves (Hall,
2005) and thus one can speculate that the odontogenic competence of ectoderm can be transferred to endoderm by cooption. This can explain observations of teeth that develop
from an endoderm-covered lining in extant vertebrates.
Regarding the principle of co-option of odontogenic competence (Smith, 2003; Fraser et al., 2004), there is thus an
agreement between the proponents of the inside-out and the
outside-in hypotheses.
Intermediate stages between dermal denticles and teeth
An argument raised to dispute the homology of dermal denticles and teeth is the supposed lack of morphologically
intermediate forms between dermal denticles and teeth
located in the oropharyngeal cavity (Smith and Coates,
1998). Indeed, if a dermal element (i.e. odontode) becomes
modified in the course of evolution, one expects to find
intermediate stages (Hall and Kerney, 2012). Different from
what the inside-out hypothesis assumes, intermediate stages
exist (Botella et al., 2007). Daniel (1934) describes the transition of placoid scales (= dermal denticles) into teeth in the
extant shark of the genus Heptanchus. A recent study by
Blais et al. (2011) shows intermediate forms between head
scales and teeth in an early Devonian eugnathostome
(Acanthodian). According to Blais et al. (2011) scales that
develop in closer proximity to the mouth are modified and
become extremely tooth-like. Moreover, in every detail the
similarity of these scales to teeth suggests that the two elements are the result of the same developmental processes,
indicative for the existence of a field of gene expression near
the mouth margin in which scales can be transformed into
teeth. The presence of extra-oral teeth in several teleost species (Arratia, 1990; Sire, 2001; Sire and Allizard, 2001)
further demonstrates the existence of a field of odontogenic
gene expression outside the mouth margin in extant
640
vertebrates. Blais et al. (2011) conclude from their studies
that their unequivocal example for transitional forms
between dermal scales and teeth removes one of the chief
objections to the outside-in hypothesis for the origins of
teeth in jawed vertebrates.
Outside-in against inside-out: the different use of the homology
concept
Homology is the hierarchical foundation of all biology and
we invoke homology whenever we compare two or more
biological units (Hall, 2003). The discussion about the evolutionary origin of teeth reveals a different use of the
homology concept. Comparative anatomists and embryologists established the homology concept in pre-Darwinian
times. Eventually the evolutionary theory was able to provide a rational explanation for the existence of homologous
structures (Hall, 2014; in this volume). Subsequently, based
on the diagnosis of homology, it was possible to establish
phylogenetic trees (Brigandt and Griffiths, 2007). It has
been a valid approach since to investigate the homology of
two characters without being upfront interested in cladogenetic relationships (Schmitt, 1989). Molecular biologists that
extend the homology concept to proteins and genes have
followed this approach (Griffiths, 2007). Homology is established based either on operational criteria or on a taxic
conception (Griffiths, 2007). The operational criteria regard
organs or structures as homologous with increasing certainty (i) if they share the position in relation to other
structures, (ii) if they share specific qualities (e.g. microstructure, biochemical composition, gene expression patterns) and (iii) if intermediate stages exist, be it ontogenetic
or phylogenetic (Remane, 1952; Futuyma, 1998; Ridley,
2004; Zachos and Hoßfeld, 2006; Schultze and Arratia,
2013). Homologous structures need not meet all criteria.
Homologous structures can develop through different pathways because development evolves (Hall, 2003). Intermediate stages can be lacking because the fossil record is
incomplete (Hall and Kerney, 2012). The position of a
structure in relation to other structures can change. For
example, pelvic fins of advanced teleost fish are now located
in front of the pectoral fins (Drucker and Lauder, 2002).
Teeth and dermal denticles are, however, arguably prime
examples for structures that meet operational homology criteria. The idea underlying the taxic concept of homology
has been summarized by Wake (1999, 2003): homology is
not evidence for evolution. Homology is the anticipated
and expected consequence of evolution. Support for the
inside-out hypothesis is drawn from the taxic homology
concept. A cladistic analysis that, for example, assigns conodonts to the vertebrates or even to the gnathostomes is
regarded as valid evidence that teeth evolved prior to the
dermal skeleton, more than once, and are not homologous
to odontodes (Smith, 2003). Adherents of the outside-in
hypothesis argue that based on operational criteria, homology between teeth and odontodes is firmly established.
Conodont elements do not meet these criteria (Turner et al.,
2010; Murdock et al., 2013), one reason why the position
of conodonts in the vertebrate tree is doubtful.
P. E. Witten, J.-Y. Sire and A. Huysseune
Hegelian dialectics: thesis-antithesis-synthesis
Paleontological, developmental, morphological, structural,
biochemical and molecular data strongly support the homology of dermal denticles and teeth. Still, the unity of dermal
denticles and teeth has been challenged during the last 15
years. The discussion about the more recent inside-out
hypothesis and the traditional outside-in hypothesis has triggered several studies, all of which provide evidence for the
original outside-in hypothesis, for the unity of teeth, odontodes and dermal denticles. The argument that dermal denticles and teeth lack intermediate stages has been refuted by
Blais et al. (2011) who demonstrate tooth-like scales in early
Devonian eugnathostomes. The argument that fundamentally
different patterning mechanisms establish positions of teeth
and dermal denticles has been rejected (Qu et al., 2013).
Huysseune et al. (2009, 2010) and R€
ucklin et al. (2012) have
emphasized that one should not remove the tooth-status
from oral teeth based on the assumed lack of a dental lamina. Consequently, the identification of oral cusps in placoderms by R€
ucklin et al. (2012) as teeth opposes the
argument that teeth derive from endodermal pharyngeal
tooth whorls. The now undisputed fact that conodont mineralized elements are unrelated to vertebrate teeth and dermal
denticles (Murdock et al., 2013) has removed another argument for an endodermal, and dermal skeleton-independent,
evolution of teeth (Turner et al., 2010). Mechanisms by
which ectoderm-derived teeth can acquire a pharyngeal position have been proposed by Huysseune et al. (2009, 2010). In
hindsight it appears that the discussion about the origin of
teeth went through a complete round of Hegelian dialectics.
We believe that the origin of teeth from dermal denticles
(odontodes) is again firmly established. Thus, there is also no
need for the assumptions that teeth may have evolved convergently from endodermal and from ectodermal locations
(‘inside and out’, Fraser et al., 2010; Fraser and Smith,
2011). The past discussion about the origin of teeth in vertebrates has, however, triggered exciting and ongoing research
about the mechanisms of tooth development, replacement
and patterning.
Acknowledgements
We are very thankful to Brian K. Hall (Dalhousie University, Halifax, Canada) and Philip C. J. Donoghue (University
of Bristol, UK) for reviewing this manuscript and for providing insightful advice for improvements. The final manuscript
remains of course entirely the responsibility of the authors.
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Author’s address: Paul Eckhard Witten, Ghent University, Biology
Department L, Ledeganckstraat 35, B-9000 Ghent,
Belgium.
E-mail: [email protected]