Tooth shape in teleosts and its link to tooth spacing and replacement

2018·1.7 MB·English

by  Huysseune, A

Tooth shape in teleosts and its link to tooth spacing
and replacement
by
Ann Huysseune* & P. eckhard Witten (1)
Abstract. – teeth continue to be in the focus in many paleontological and neontological disciplines, and their
morphological characters, histological structure and mode of attachment are the subject of ongoing studies. in
this review, we elaborate on tooth shape. We first highlight the progress that was made over the last two dec-
ades in understanding the mechanisms that determine the shape of a tooth. We then describe the often dramatic
changes that tooth shape undergoes in ontogeny. Finally, we discuss characters of the dentition to which tooth
shape may be intimately linked: tooth number and thus tooth spacing, as well as tooth replacement. While litera-
ture about various non-mammalian vertebrates is considered, this review focuses on the highly speciose teleost
group.
Résumé. – La forme des dents des téléostéens et sa relation avec leur espacement et leur remplacement.
© SFI
Received: 19 Jul. 2017 Les dents sont toujours au cœur de nombreuses études paléontologiques et néontologiques et leurs caractères
Accepted: 7 Dec. 2017
morphologiques, leur structure histologique et leur mode d’attachement sont l’objet d’études renouvelées. La
Editor: O. Otero
revue présentée ici s’intéresse à la forme des dents. elle débute par la présentation des progrès réalisés au cours
des vingt dernières années dans la compréhension des mécanismes de détermination de la forme d’une dent. Puis
ce sont les changements, parfois radicaux, que subit la forme de la dent au cours de l’ontogénie, qui sont décrits.
Finalement, la discussion porte sur les caractères de la dentition auxquels la forme des dents est probablement
Key words
intimement liée : le nombre des dents et donc leur espacement, et leur renouvellement. si la littérature concer-
tooth morphology
nant l’ensemble des vertébrés non mammifères est considérée, la revue se concentre sur le groupe ultra-diversifié
Cusp
des téléostéens.
tooth replacement
Polyphyodonty
teleosts
teeth evolved from odontodes and other species, the shape of the teeth is not correlated with diet,
are part of the dermal skeleton (Mai- and probably reflects phylogenetic relationships (e.g. sparids,
sey, 1988; sire and Huysseune, 2003; Linde et al., 2004). Various explanations have been proposed
Huysseune et al., 2009). their structure and composition for the lack of similarity in tooth shape between species with
were studied in a series of detailed and beautifully illustrated similar diets: different feeding strategies, even for the same
papers by Meunier and co-workers (e.g. Meunier, 1983; sire food category, the importance of other food properties, mul-
et al., 1987; Francillon-Vieillot et al., 1990; sire and Meu- tiple tasks performed by a single tooth, or even the lack of a
nier, 1993; Meunier and Zylberberg, 1999; Brito et al., 2000; role in predation (Linde et al., 2004). Part of the explanation
Daget et al., 2001; Cuny et al., 2010). Many paleontological may also lie in pleiotropic effects of genes involved in shaping
and neontological disciplines focus on teeth. Because of their the tooth (Albertson et al., 2003). While most studies focus on
excellent preservation, teeth are often the sole fossil remains, tooth shape, tooth attachment is obviously equally, if not more,
and their shape, as well as their histological structure, offers important for the function of teeth. Meunier and his co-work-
exquisite information on the animals that possessed them, ers have addressed the important subject of tooth attachment
and the environment in which they lived (e.g. Gayet et al., in sarcopterygians and actinopterygians in several recent stud-
2001; Cuny et al., 2010; Meunier et al., 2013). in neonto- ies (Meunier, 2015; Meunier et al., 2015a, b; Germain et al.,
logical research, tooth shape is highly valued as a character 2016). Finally, studies on teeth have been instructive in our
as such, e.g. in taxonomic and phylogenetic research (e.g. knowledge of organ morphogenesis, cytodifferentiation and
Wautier et al., 2002; Pasco-Viel et al., 2010; Ahnelt et al., pattern formation. the combination of this knowledge with
2015). the shape (as well as size) of teeth can furthermore comparative anatomical and paleontological data has given
be highly informative in an ecomorphological context (e.g. teeth a paradigmal status in evo-devo research (e.g. stock,
Aguilar-Medrano, 2017). In teleost fish, correlations between 2001; Jernvall and thesleff, 2012; tucker and Fraser, 2014).
tooth shape and diet have in some cases been endorsed (e.g. it has now become increasingly clear that the shape of
a carangid, Francillon-Vieillot et al., 1994; eretmodine cich- teeth is not a character of the dentition that is fixed or stands
lids, Rüber et al., 1999; cyprinins, Pasco-Viel et al., 2014); in alone. Rather, recent studies that have focussed on non-mam-
(1) Biology Department, Ghent university, Belgium. [[email protected]]
* Corresponding author [[email protected]]
Cybium 2018, 42(1): 19-27.
Tooth shape in teleosts Huysseune & Witten
malians have shown that tooth shape is sometimes undergo- expression as well as functional studies in teleosts, in par-
ing dramatic changes in ontogeny, and that tooth shape and ticular zebrafish, have nevertheless revealed that this may be
tooth number (and thus spacing) may be intimately linked. an oversimplification, given differences both in gene expres-
Likewise, an apparent link has surfaced between tooth shape sion and function between teleost and mammalian (mouse)
and tooth replacement. in this review, we will focus on these teeth (e.g. Jackman et al., 2004; Wise and stock, 2010).
two relationships and illuminate new insights that have been in the quest of uncovering how the development of tooth
acquired since Huysseune and sire (1998) discussed patterns shape is controlled, particular attention has been paid to how
and processes in the evolution of non-mammalian dentitions. cusps arise and shape the tooth tip (the term ‘crown’ is used
However, prior to do so, we will highlight the progress that sometimes but is avoided here because it essentially describes
has been made over the last twenty years in understanding a mammalian-type tooth surface). in mammals, a cluster of
the mechanisms that determine the shape of a tooth. While non-dividing cells, called enamel knot, is located in the enam-
we will cover literature of various non-mammalians, the el organ and acts as a signalling centre promoting proliferation
focus of this paper is on the most speciose lineage of verte- of the surrounding dental epithelium. its action entails folding
brates, the teleosts. of the epithelial-mesenchymal interface and thus the forma-
tion of a first cusp – hence the designation of primary enamel
Mechanisms underlying the acquisition of tooth shape knot. in multicuspid teeth, a secondary enamel knot appears at
An increasing number of studies has addressed the mech- the future location of each cusp (Jernvall et al., 1994; Jernvall
anisms determining tooth shape in non-mammalians. Across and thesleff, 2012). using the catshark Scyliorhinus ccaannii--
vertebrates, tooth development proceeds through essentially cula (Linnaeus, 1758), Debiais-thibaud et al. (2015) showed
the same steps, i.e. initiation, morphogenesis and cytodiffer- that, while homologous regulatory pathways are expressed
entiation (for reviews see Huysseune and sire, 1998; stock, during tooth morphogenesis in shark and mouse (shh, Bmp
2007; Davit-Béal et al., 2007; Richman and Handrigan, and Fgf), their results did not support the existence of a pri-
2011; Berkovitz and shellis, 2017). As a proof of concept, mary enamel knot in sharks. in contrast, Fraser et al. (2013),
Borday-Birraux et al. (2006) and ellis et al. (2015) could working on cichlids, took foci of expression of some devel-
synchronise specific stages during teleost tooth development opmental genes to be evidence for the existence of a primi-
(zebrafish and threespine stickleback, respectively) with the tive enamel knot-like signalling centre that controls (amongst
typical stages in mammalian tooth development, i.e. bud, cap others) cusp number. Detailed expression data with sufficient
and bell stages. not surprisingly, the genetic and molecular resolution (in particular to show expression in the inner dental
mechanisms regulating tooth development in non-mamma- epithelium) will be needed to support this hypothesis. Moreo-
lians and in mammals have revealed themselves as consid- ver, considering the small number of cells involved in form-
erably conserved. they involve signalling factors belonging ing first-generation teeth, and their first replacers, one would
to four large families of signalling molecules, i.e. shh, Fgf, have to imagine that perhaps only one cell behaves differently
Wnt, and tGF-beta families (Jernvall and thesleff, 2012), from its neighbours in terms of gene expression and cell cycle
leading Fraser et al. (2009) to propose a conserved gene characteristics to achieve relief on the tooth surface. Micro-
network for all vertebrate teeth. Detailed studies on gene ornamentations of maximally a few micrometers in size (i.e.
Figure 1. – A: Scanning electron micrograph of the pharyngeal dentition of a one month-old zebrafish (10.4 mm SL). Note
considerable differences in tooth shape in the different positions, and micro-ornamentations (arrowheads) at the tooth tip.
Anterior to the left, dorsal to the top. B: Detail of the micro-ornamentations of the tooth tip. note major cusp (asterisk), minor
cusp (arrow), and basal protuberance (arrowhead). C: transmission electron micrograph of a developing replacement tooth
in a one month-old zebrafish (9 mm S.L.). Note that the minor cusp is developing with just one odontoblast extending into it
(arrow). scale bars: A = 50 µm; B = 10 µm; C = 10 µm.
20 Cybium 2018, 42(1)
Huysseune & Witten Tooth shape in teleosts
smaller than the average cell size), such as found on the mono-
cuspid teeth in zebrafish (Wautier et al., 2001, Fig. 1), could
then be the result of the specific shape characteristics of that
cell, and/or differential deposition of dental matrix (Fig. 1C).
Handrigan and Richman (2011) and Zahradnicek et al. (2014)
described a similar situation in reptiles, where differential
deposition of enamel matrix forms cusps, thus functionally
substituting for a true primary enamel knot. in teleosts, mul-
ticuspid tooth shapes have been experimentally induced in
species possessing unicuspid teeth by upregulating Fgf and
downregulating Bmp signalling (Jackman et al., 2013). these
results are in line with the idea, tested in mice, that simple
alteration of key signalling pathways can be used to transform
a prototypical conical-shaped tooth into one with complex
morphology (Plikus et al., 2005). Disrupted eda signalling,
another signalling pathway next to the four mentioned above,
affects tooth number and shape in mammals (Kangas et al.,
2004; tucker et al., 2004), as well as in selected teleosts, such
as in zebrafish (Harris et al., 2008). in medaka, disrupted eda
signalling only caused changes in tooth number, not in shape
(Atukorala et al., 2010). However, high-resolution imaging or
sophisticated morphometric methods are sometimes required
to establish shape differences, especially when dealing with
small teeth of relatively simple shape (e.g. Clemen et al., 1998;
Wautier et al., 2002). Likewise, the use of X-ray tomography
can reveal details of the (inner) spatial morphology that would
otherwise remain unnoticed (Germain et al., 2016).
Ontogenetic changes in tooth shape
teeth in non-mammalians, and particularly in teleosts,
are often claimed to be of a simple shape throughout the
dentition (so-called homodont dentition, i.e. similar-shaped
teeth making up the entire dentition). this is clearly wrong.
Many non-mammalians, including teleosts, possess teeth of Figure 2. - the heterodont dentition of an advanced perciform tel-
a far more diverse, and often more complex shape (Peyer, eost, the wolffish Anarhichas sp., according to Owen (1840-1845).
1968; Berkovitz and shellis, 2017). For example, the shape
can range from the commonly occurring monocuspid teeth, of sufficient data on a population level prevents us howev-
whether slender or sturdy, rod- or peg-like, to bicuspid teeth er to make statements on how common this observation is.
forming interlocking series, as in some coral reef fish (Streit in addition, tooth shape can be extremely different among
et al., 2015), Z-shaped with a curved bicuspid crown, as in closely related species (e.g. the cichlid tribe of eretmodini,
scraping catfish (Geerinckx et al., 2007), tri- to pentacuspid Rüber et al., 1999; Vandervennet et al., 2006; the cyprinid
teeth, as in the characid genus Astyanax (Marinho and Lima, subfamily of the Poropuntiini; Pasco-Viel et al., 2014), or
2009), enlarged caniniform fang-like teeth, as in Lophius pis- even within and among populations of a single species, e.g.
catorius Linnaeus, 1758 (Meunier, 2015), delivering venom in the cichlid Metriaclima zebra (Boulenger, 1899) (streel-
in some cases, as in fangblennies (Casewell et al., 2017), up man et al., 2007).
to overt heterodonty, as in the Atlantic wolffish (Anarhichas Despite complex adult tooth shape, the first teeth in the
lupus Linnaeus, 1758) (Bemis and Bemis, 2015) (Fig. 2). dentition are usually conical, slightly curved, monocuspid
Cichlid fishes are notorious for their tooth shape diversity teeth (sire et al., 2002). Because teeth cannot change shape
(Fryer and iles, 1972; Barel et al., 1977; Huysseune, 1995; once fully formed – they can only wear off – substantial tooth
Albertson and Kocher, 2006). However, even supposedly shape changes, such as from monocuspid to tri- or multicuspid
‘simple’ teeth of the widespread laboratory ‘fish’, Danio teeth, can clearly only be achieved through successive (often
rerio (Hamilton, 1822), can have a far more complex shape multiple) cycles of tooth replacement (Witten and Hall, 2015)
upon closer inspection (Wautier et al., 2001) (Fig. 1). Lack (Fig. 3). such changes are thus essentially restricted to non-
Cybium 2018, 42(1) 21
Tooth shape in teleosts Huysseune & Witten
Figure 3. - the upper jaw dentition in three different life stages of Eretmodus cf. cyanostictus (lineage A) (A-C) (11.4 mm
SL, 23.4 mm SL and 51.0 mm S.L., resp.) and magnifications of an individual tooth in the respective dentition (A’-C’).
D: Lower jaw of the specimen used in (B, B’), showing monocuspid teeth, formed extramedullary (arrowhead), at the end
of a row of spatulate teeth, displaying intramedullary replacement. D’: Detail of the last spatulate tooth (arrow) showing
replacement tooth forming intramedullary below (asterisk). scale bars: A, B’, D’ = 100 µm; A’ = 15 µm; B, C = 500 µm;
C’, D = 200 µm.
mammalians, that is, vertebrates that are capable of renewing size, conical shape, atubular dentine, and small pulp cavity
their teeth lifelong. in the Mexican tetra Astyanax mexica- without capillaries and blood vessels. this type was found in
nus (De Filippi, 1853), the transition from monocuspid to actinopterygians, dipnoans, and urodeles, and was observed
multicuspid during ontogeny is abrupt: monocuspid teeth to coincide with the occurrence of a short embryonic period
are replaced by bi- or tricuspid teeth over one replacement in the respective species. the authors considered this con-
cycle, and subsequently by teeth with more cusps over the served simple shape to be an ancestral character of gnath-
next cycles (trapani et al., 2005). Morphological changes in ostome teeth. yet, the study also highlighted the presence of
tooth shape must not necessarily proceed over one tooth gen- another type of first-generation teeth (termed type 2). These
eration, but can also happen gradually, as in carangids (Fran- have in common that they represent miniature versions of
cillon-Vieillot et al., 1994) or in eretmodine cichlids (Fig. 3). adult teeth. they were found to be generally larger than the
interestingly, Machado-evangelista et al. (2015) observed an first type, with more complex shapes, tubular dentine, and a
opposite ontogenetic gradient in another characiform, Lepo- large pulp cavity containing blood vessels. these teeth were
rinus reticulatus Britski & Garavello, 1993: from tricuspid observed in chondrichthyans, squamates, and crocodiles,
teeth in small specimens, to spatula-shaped teeth in large taxa which all share an extended embryonic period.
specimens through an increasing level of fusion of cusps. Considering recent findings indicating conservation of
the common knowledge across ichthyologists and her- tooth gene expression between initial and replacement teeth
petologists, that the first teeth in a dentition are often coni- (Hulsey et al., 2016), the question remains how more com-
cal, slightly curved, monocuspid teeth, was crystallized in a plex tooth shapes develop in species that start their develop-
paper that analysed and compared size, shape, and structure ment with monocuspid teeth. this question was tackled from
of the first-generation teeth in a wide sample of non-mam- an evolutionary developmental viewpoint by streelman et al.
malians (chondrichthyans as well as osteichthyans) (sire et (2003), and streelman and Albertson (2006), taking advan-
al., 2002). this study confirmed the universal presence of tage of the diversity in cichlid tooth shapes. they proposed
simple-shaped teeth, termed type 1, characterized by a small a model in which tooth shape is determined by the dynamic
22 Cybium 2018, 42(1)
Huysseune & Witten Tooth shape in teleosts
ratio between molecular “cusp-activators” that promote cell link between tooth number and tooth shape. Whilst this claim
differentiation and “cusp-inhibitors” that counteract the awaits testing on a wider range of teleosts, it will also need
activator and thus promote epithelial and mesenchymal cell to be reconciled with the authors’ own and other authors’
growth. in their model, these molecules are expressed/secret- observations regarding spacing of the first-generation teeth.
ed from transient-appearing, epithelial signalling centres, indeed, the difference in bmp expression domain around the
similar to the enamel knots of mammalian molars. Accord- developing first-generation teeth in the three cichlid species
ing to streelman et al. (2003), unicuspid cichlid teeth would studied in streelman and Albertson (2006) is at odds with the
then result from a high amount of cusp-inhibitor, secreted by fact that these domains prefigure the presence of simple coni-
the signalling centre, preventing secondary cusp formation. cal teeth in all three species. Likewise, the first teeth on the
in species with a multicuspid adult dentition, the concentra- Atlantic salmon dentary (between odd positions) are initiated
tion of inhibitor would decrease with tooth turnover, thus at twice the distance necessary for the initiation of adjacent
allowing the formation of more cusps. Vandervennet et al. teeth further back in the row, whilst their size and shape is
(2006) used this model to explain the ontogenetic transition approximately similar (Huysseune et al., 2007). in medaka
from conical to spatulate teeth in the cichlid Eretmodus cf. too, tooth spacing appears not to be coupled to tooth shape
cyanostictus Boulenger, 1898 (lineage A). they proposed (Atukorala et al., 2010). thus, despite evidence discussed
that the observed unequal growth of the epithelium and/or above, that the molecular control of tooth and cusp number
the mesenchyme could be the result of an asymmetric field are somehow linked, the subtleties of this regulation are not
of inhibition, giving rise to an asymmetrically developing yet well understood. Furthermore, there is a growing incen-
spatulate tooth. thus, the spatulate shape could be consid- tive to shift the research focus to changes in cis-regulation of
ered the mildest possible expression of a bicuspid tooth. important developmental genes. indeed, Cleves et al. (2014)
A reverse genetics approach on Lake Malawi cichlid spe- discovered cis-regulatory changes of expression level of
cies led Albertson and Kocher (2006) to suggest that cusp the gene bmp6 to underlie an increase in tooth number in a
number may be largely determined by a single genetic fac- derived benthic population of threespine stickleback. it would
tor. One last consideration concerns the role of thyroid hor- be interesting to investigate whether there is a co-occurrence
mone in establishment of tooth shape. Changing thyroid of tooth shape changes.
hormone levels at metamorphosis have been associated with Another line of investigations suggests that tooth distri-
tooth loss (e.g. in conger eel, Conger myriaster (Brevoort, bution in actinopterygians is under control of retinoic acid
1856), Kawakami et al., 2003), or with the appearance of signalling. seritrakul et al. (2012) could experimentally
(new) teeth (e.g. in the Hawaiian stream goby Sicyopterus expand the dentition in zebrafish after administering exog-
stimpsoni (Gill, 1860), schoenfuss 1997). these transitions enous retinoic acid (RA), suggesting this to be the result of
are often linked to a change in feeding mode, particularly a homeotic transformation. this interpretation was revised
noticeable in tropical reef fishes (McCormick et al., 2002). after further experiments by Gibert et al. (2015), leading
Whether thyroid hormone can directly affect the process of these authors to suggest that tinkering with endogenous RA
odontogenesis at a particular tooth locus to produce a differ- levels may be a way how evolution achieved changes in the
ently shaped tooth is not known at present, but not unlikely. dentition in cyprinids. Whether there is co-occurrence of
indeed, it has been well established that changing thyroid changes in tooth number and tooth shape during cyprinid
hormone levels at metamorphosis affect tooth shape in sala- evolution, and if a change in RA signalling is the underlying
manders, in particular cusp morphology and enamel thick- mechanism, is not known at present.
ness (reviewed in Davit-Béal et al., 2007).
A link between tooth shape and replacement
A link between tooth shape and tooth number? Because teeth cannot change their shape once fully
streelman et al. (2003) and streelman and Albertson formed, it is clear that tooth replacement is required to
(2006) suggested that their model of cusp activators and achieve a complex adult tooth shape out of simple coni-
inhibitors, discussed above, can explain the empirical rela- cal teeth in embryonic and post-embryonic stages. the link
tionship between tooth number and tooth shape. thus, between tooth shape and replacement nevertheless extends
monocuspid teeth present a wider spacing, while multicus- beyond this association, thereby possibly involving common
pid teeth are set closer. This has been confirmed, e.g. for dif- molecular signals (Fraser et al., 2013). Indeed, first-genera-
ferent populations of the cichlid Metriaclima zebra (streel- tion, monocuspid teeth always develop on the surface of the
man et al., 2007) and for different species of characiforms dentigerous bone, irrespective of whether later tooth genera-
(trapani et al., 2005, and references therein). Jackman et al. tions develop intramedullary, a condition found in advanced
(2013) manipulated Fgf and Bmp signalling in zebrafish and teleosts (pers. obs.; see also Francillon-Vieillot et al., 1994;
in the Mexican tetra and not only obtained multicuspid, but trapani, 2001; trapani et al., 2005). interestingly, this appears
also supernumerary teeth in both species, further supporting a to hold also when new teeth are added at the end of a row of
Cybium 2018, 42(1) 23
Tooth shape in teleosts Huysseune & Witten
teeth that have already shifted from extra- to intramedullary inspiration and knowledge for PeW. the authors thank the anony-
mous reviewers for their comments.
development (Fig. 3). Besides the above association between
tooth shape and the morphological context, in which replace-
ment takes place (extra- or intramedullary), the capacity of
RefeRenCes
undergoing (multiple) replacement cycles also allows a level
of phenotypic plasticity in the dentition that is not possible AGuiLAR-MeDRAnO R., 2017. - ecomorphology and evolution
in mammals, which have at most one replacement event. in of the pharyngeal apparatus of benthic damselfishes (Pomacen-
tridae, subfamily stegastinae). Mar. Biol., 164: 21.
the cichlid Astatoreochromis alluaudi Pellegrin, 1904, the
AHneLt H., HeRDinA A.n. & MetsCHeR B.D., 2015. - unu-
pharyngeal jaws start to diverge in shape from 40 mm sL
sual pharyngeal dentition in the African Chedrin fishes (Tele-
onwards, depending on whether the animals feed on a soft or ostei: Cyprinidae): Significance for phylogeny and character
hard diet (Hoogerhoud, 1986). A hard diet elicits the forma- evolution. Zool. Anz., 255: 85-102.
tion of large, molariform teeth, a softer diet that of more, but ALBeRtsOn R.C. & KOCHeR t.D., 2006. - Genetic and devel-
opmental basis of cichlid trophic diversity. Heredity, 97: 211-
less sturdy, teeth (Huysseune 1995, 2000). For both diets, a
221.
one-for-one-replacement was assumed. Maintenance of tooth
ALBeRtsOn R.C., stReeLMAn J.t. & KOCHeR t.D., 2003. -
numbers and increase of tooth size in hard-food specimens Genetic basis of adaptive shape differences in the cichlid head.
were then hypothesized to be achieved by expansion of the J. Hered., 94(4): 291-301.
tooth-bearing region and possibly by closer spacing of the AtuKORALA A.D., inOHAyA K., BABA O., tABAtA M.J.,
RAtnAyAKe R.A.R.K., ABDuWeLi D., KAsuGAi s.,
teeth. increase of tooth numbers in the soft-food specimens
MitAni H. & tAKAnO y., 2010. - scale and tooth pheno-
could have been achieved through the establishment of new types in medaka with a mutated ectodysplasin-A receptor:
tooth loci at the margins of the dentigerous area. Gunter and implications for the evolutionary origin of oral and pharyngeal
teeth. Arch. Histol. Cytol., 73: 139-148.
colleagues have started to examine the molecular underpin-
BAReL C.D.n., VAn OiJen M.J.P., Witte F. & Witte-MAAs
nings of this plasticity, focusing nevertheless on the lower
e.L.M., 1977. - An introduction to the taxonomy and morphol-
pharyngeal jaw rather than on the teeth (Gunter et al., 2013; ogy of the haplochromine Cichlidae from Lake Victoria. Neth.
Gunter and Meyer, 2014; schneider et al., 2014). they identi- J. Zool., 27: 333-389.
fied 187 genes whose expression differs in response to hard BeMis K.e. & BeMis W.e., 2015. - Functional and developmen-
tal morphology of tooth replacement in the Atlantic Wolffish,
and soft diets, including immediate early genes, extracellular
Anarhichas lupus (teleostei: Zoarcoidei: Anarhichadidae).
matrix genes and inflammatory factors (Gunter et al., 2013).
Copeia, 103(4): 886-901.
these authors furthermore proposed that pleiotropic genes
BeRKOVitZ B.K.B. & sHeLLis R.P., 2017. - the teeth of non-
are likely to guide the development of both teeth and jaws. Mammalian Vertebrates. 354 p. san Diego: elsevier science
the challenge will be to reconcile such a proposal with the Publishing Co.
idea that teeth and jaws (whether oral, or pharyngeal) develop BORDAy-BiRRAuX V., VAn DeR HeyDen C., DeBiAis-
tHiBAuD M., VeRReiJDt L., stOCK D.W., Huysseune
to a large extent independent from each other (schilling et al.,
A. & siRe J.y., 2006. - expression of Dlx genes during the
1996; Rücklin et al., 2012; Paradis et al., 2013; Hammer et development of the zebrafish pharyngeal dentition: evolution-
al., 2016). ary implications. Evol. Dev., 8(2): 130-141.
BRitO P.M., MeunieR F.J. & GAyet M., 2000. - the morphol-
ogy and histology of the scales of the Cretaceous gar Obaich-
Conclusions and perspectives
thys (Actinopterygii, Lepisosteidae): phylogenetic implica-
We have critically assessed the relationship between tions. C. R. Acad. Sci. Paris, Sér. IIA, 331(12): 823-829.
tooth shape and tooth number, and have highlighted the CAseWeLL n.R., VisseR J.C., BAuMAnn K. et al. [24
advantages that continuous tooth renewal generates, namely authors], 2017. - the evolution of fangs, venom, and mimicry
systems in blennyfishes. Curr. Biol., 27: 1184-1191.
a shift in where replacement teeth can develop (from extra-
CLeMen G., BARtsCH P. & WACKeR K., 1998. - Dentition and
to intramedullary replacement in advanced teleosts), and
dentigerous bones in juveniles and adults of Polypterus senega-
ample possibilities for phenotypic plasticity. We still have lus (Cladistia, Actinopterygii). Ann. Anat., 180: 211-221.
a long way to go before we will fully understand how the CLeVes P.A., eLLis n.A., JiMeneZ M.t., nuneZ s.M.,
acquisition of tooth shape in teleosts is regulated. We need sCHLuteR D., KinGsLey D.M. & MiLLeR C.t., 2014. -
evolved tooth gain in sticklebacks is associated with a cis-reg-
to understand how micro-ornamentations are produced on
ulatory allele of Bmp6. PNAS USA, 111(38): 13912-13917.
the surface of teeth of even rather simple shape, and what
Cuny G., COBBett A.M., MeunieR F.J. & BentOn M.J.,
controls an increasingly more complex tooth shape during 2010. - Vertebrate microremains from the early Cretaceous of
ontogeny. Likewise, dental sexual dimorphism in teleosts southern tunisia. Geobios, 43: 615-628.
and its (sex-dependent) temporal plasticity are exciting DAGet J., GAyet M., MeunieR F.J. & siRe J.y., 2001. - Major
research subjects that need to be further explored. discoveries on the dermal skeleton of fossil and recent polypter-
iforms: a review. Fish Fish., 2: 113-124.
DAVit-BÉAL t., CHisAKA H., DeLGADO s. & siRe J.y., 2007.
Acknowledgements. – this paper is dedicated to F.J. Meunier, - Amphibian teeth: current knowledge, unanswered questions,
first teacher in teleost skeletal biology to AH and lifelong source of and some directions for future research. Biol. Rev., 82: 49-81.
24 Cybium 2018, 42(1)
Huysseune & Witten Tooth shape in teleosts
DeBiAis-tHiBAuD M., CHiORi R., enAuLt s., OuLiOn s., HARRis M.P., ROHneR n., sCHWARZ H., PeRAtHOneR s.,
GeRMOn i., MARtinAnD-MARi C., CAsAne D. & BOR- KOnstAntiniDis P. & nÜssLein-VOLHARD C., 2008. -
DAy-BiRRAuX V., 2015. - tooth and scale morphogenesis in Zebrafish eda and edar mutants reveal conserved and ancestral
shark: an alternative process to the mammalian enamel knot roles of ectodysplasin signaling in vertebrates. PLoS Genet., 4:
system. BMC Evol. Biol., 15: 292. e1000206.
HOOGeRHOuD R.J.C., 1986. - taxonomic and ecological aspects
eLLis n.A., GLAZeR A.M., DOnDe n.n., CLeVes P.A., AGO-
of morphological plasticity in molluscivorous haplochromines
GLiA R.M. & MiLLeR C.t., 2015. - Distinct developmental
(Pisces, Cichlidae). Ann. Mus. R. Afr. Cent. Sci. Zool., 251:
genetic mechanisms underlie convergently evolved tooth gain
131-134.
in sticklebacks. Development, 142: 2442-2451.
HuLsey C.D., FRAseR G.J. & MeyeR A., 2016. - Biting into
FRAnCiLLOn-VieiLLOt H., De BuFFRÉniL V., CAstAnet the genome to phenome map: Developmental genetic modular-
J., GÉRAuDie J., MeunieR F.J., siRe J.y., ZyLBeRBeRG ity of cichlid fish dentitions. Integr. Comp. Biol., 1-16.
L. & De RiCQLÉs A., 1990. - Microstructure and mineraliza-
Huysseune A., 1995. - Phenotypic plasticity in the lower pha-
tion of vertebrate skeletal tissues. In: skeletal Biomineraliza-
ryngeal jaw dentition of Astatoreochromis alluaudi (teleostei:
tion: Patterns, Processes and evolutionary trends, Vol. 1 (Cart- Cichlidae). Arch. Oral Biol., 40: 1005-1014.
er J.G., ed.), pp. 471-530. new york: Van nostrand Reinhold.
Huysseune A., 2000. - Developmental plasticity in the dentition
FRAnCiLLOn-VieiLLOt H., tReBAOL L., MeunieR F.J. & of a heterodont polyphyodont fish species. In: Development,
sLeMBROuCK J., 1994. - Histological study of odontogene- Function and evolution of teeth (teaford M., smith M. & Fer-
sis in the pharyngeal jaws of Trachinotus teraia (Cuvier & guson M., eds), pp. 231-241. Cambridge: Cambridge univ.
Valenciennes, 1832) (Osteichthyes, teleostei, Carangidae). J. Press.
Morphol., 220(1): 11-24. Huysseune A. & siRe J.y., 1998. - evolution of patterns and
FRAseR G.J., HuLsey C.D., BLOOMQuist R.F., uyesuGi processes in teeth and tooth-related tissues in non-mammalian
K., MAnLey n.R. & stReeLMAn J.t., 2009. - An ancient vertebrates. Eur. J. Oral Sci., 106: 437-481.
gene network is co-opted for teeth on old and new jaws. PLoS Huysseune A., HALL B.K. & Witten P.e., 2007. - establish-
Biol., 7(2): e1000031. ment, maintenance and modifications of the lower jaw dentition
of wild Atlantic salmon (Salmo salar L.) throughout its life
FRAseR G.J., BLOOMQuist R.F. & stReeLMAn J.t., 2013. -
cycle. J. Anat., 211: 471-487.
Common developmental pathways link tooth shape to regener-
Huysseune A., siRe J.y. & Witten P.e., 2009. - evolution-
ation. Dev. Biol., 377: 399-414.
ary and developmental origins of the vertebrate dentition. J.
FRyeR G. & iLes t.D., 1972. - the Cichlid Fishes of the Great Anat., 214: 465-476.
Lakes of Africa. 641 p. edinburgh: Oliver & Boyd.
JACKMAn W.R., DRAPeR B.W. & stOCK D.W., 2004. - Fgf-
GAyet M., MARsHALL L.G., seMPeRe t., MeunieR F.J., signaling is required for zebrafish tooth development. Dev.
CAPPettA H. & RAGe J.C., 2001. - Middle Maastrichtian Biol., 274: 139-157.
vertebrates (fishes, amphibians, dinosaurs and other reptiles, JACKMAn W.R., DAVies s.H., LyOns D.B., stAuDeR C.K.,
mammals) from Pajcha Pata (Bolivia). Biostratigraphic, palae- DentOn-sCHneiDeR B.R., JOWDRy A., AiGLeR s.R.,
oecologic and palaeobiogeographic implications. Palaeogeogr., VOGeL s.A. & stOCK D.W., 2013. - Manipulation of Fgf
Palaeoclim., Palaecol., 169: 39-68. and Bmp signaling in teleost fishes suggests potential pathways
for the evolutionary origin of multicuspid teeth. Evol. Dev.,
GeeRinCKX t., De POORteR J. & ADRiAens D., 2007. -
15(2): 107-118.
Morphology and development of teeth and epidermal brushes
in Loricariid Catfishes. J. Morphol., 268: 805-814. JeRnVALL J. & tHesLeFF i., 2012. - tooth shape formation and
tooth renewal: evolving with the same signals. Development,
GeRMAin D., MOnDÉJAR-FeRnÁnDeZ J. & MeunieR F.J.,
139: 3487-3497.
2016. - the detection of weakly developed plicidentine in tele-
JeRnVALL J., Kettunen P., KARAVAnOVA i., MARtin L.B.
ost teeth using 3D tomography. Cybium, 40(1): 75-82.
& tHesLeFF i., 1994. - evidence for the role of the enamel
GiBeRt y., sAMARut e., PAsCO-VieL e., BeRnARD L., knot as a control center in mammalian tooth cusp formation:
BORDAy-BiRRAuX V., sADieR A., LABBe C., ViRiOt L. non-dividing cells express growth stimulating Fgf-4 gene. Int.
& LAuDet V., 2015. - Altered retinoic acid signalling under- J. Dev. Biol. 38, 463-469.
pins dentition evolution. Proc. R. Soc. B, 282: 20142764. KAnGAs A.t., eVAns A.R., tHesLeFF i. & JeRnVALL J.,
GunteR H. & MeyeR A., 2014. - Molecular investigation of 2004. - nonindependence of mammalian dental characters.
mechanical strain-induced phenotypic plasticity in the ecologi- Nature, 432: 211-214.
cally important pharyngeal jaws of cichlid fish. J. Appl. Ichthy- KAWAKAMi y., tAnDA M., ADACHi s. & yAMAuCHi K.,
ol., 30(4): 630-635. 2003. - Characterization of thyroid hormone receptor a and b
in the metamorphosing Japanese conger eel, Conger myriaster.
GunteR H.M., FAn s., XiOnG F., FRAnCHini P., FRuCiAnO
Gen. Comp. Endocrinol., 132: 321-332.
C. & MeyeR A., 2013. - shaping development through
mechanical strain: the transcriptional basis of diet-induced phe- LinDe M., PALMeR M. & GOMeZ-ZuRitA J., 2004. - Differ-
ential correlates of diet and phylogeny on the shape of the pre-
notypic plasticity in a cichlid fish. Mol. Ecol., 22(17): 4516-
maxilla and anterior tooth in sparid fishes (Perciformes: Spari-
4531.
dae). J. Evol. Biol., 17: 941-952.
HAMMeR C.L., AtuKORALA A.D.s. & FRAnZ-ODenDAAL
MACHADO-eVAnGeListA M., esGuiCeRO A.L.H., ARCiFA
t.A., 2016. - What shapes the oral jaws? Accommodation of
M.s. & PeReiRA t.n.A., 2015. - Diet and ecomorphology of
complex dentition correlates with premaxillary but not man- Leporinus reticulatus (Characiformes: Anostomidae) from the
dibular shape. Mech. Dev., 141: 100-108. upper Rio Juruena, Mt, Brazil: ontogenetic shifts related to the
HAnDRiGAn G.R. & RiCHMAn J.M., 2011. - unicuspid and feeding ecology. Acta Amazon., 45(4): 383-392.
bicuspid tooth crown formation in squamates. J. Exp. Zool. MAisey J.G., 1988. - Phylogeny of early vertebrate skeletal induc-
(Mol. Dev. Evol.), 316: 598-608. tion and ossification patterns. Evol. Biol., 22: 1-36.
Cybium 2018, 42(1) 25
Tooth shape in teleosts Huysseune & Witten
MARinHO M.M.F. & LiMA F.C.t., 2009. - Astyanax ajuricaba: a sCHneiDeR R.F., Li y., MeyeR A. & GunteR H.M., 2014. -
new species from the Amazon basin in Brazil (Characiformes: Regulatory gene networks that shape the development of adap-
Characidae). Neotrop. Ichthyol., 7(2): 169-174. tive phenotypic plasticity in a cichlid fish. Mol. Ecol., 23: 4511-
4526.
McCORMiCK M.i., MAKey L. & DuFOuR V., 2002. - Compar-
ative study of metamorphosis in tropical reef fishes. Mar. Biol., sCHOenFuss H.L., 1997. - Metamorphosis of the Hawaiian
141: 841-853. stream Goby Sicyopterus Stimpsoni: A structural, Functional,
and Behavioral Analysis. Lsu Historical Dissertations and
MeunieR F.J., 1983. - Les tissus osseux des Ostéichthyens : struc-
theses. 6595.
ture, genèse, croissance et évolution. Ph.D. dissertation, univ.
of Paris. seRitRAKuL P., sAMARut e., LAMA t.t., GiBeRt y., LAu-
Det V. & JACKMAn W.R., 2012. - Retinoic acid expands the
MeunieR F.J., 2015. - new data on the attachment of teeth in the
evolutionarily reduced dentition of zebrafish. FASEB J., 26:
Angler fish Lophius piscatorius (Actinopterygii; teleostei;
5014-5024.
Lophiidae). Cah. Biol. Mar., 56(2): 97-104.
siRe J.y. & Huysseune A., 2003. - Formation of dermal skele-
MeunieR F.J. & ZyLBeRBeRG L., 1999. - the structure of the
tal and dental tissues in fish: a comparative and evolutionary
outer components of the scales of Latimeria chalumnae (sar-
approach. Biol. Rev., 78: 219-249.
copterygii : Actinistia : Coelacanthidae) revisited using scan-
ning and transmission electron microscopy. In: Proceedings of SIRE J.Y. & MEUNIER F.J., 1993. - Superficial ornamentation and
the 5th Indo-Pacific Fish Conference1997, Nouméa (Seret B. & structure of the osseous dermal plates in some armored sil-
sire J.y., eds), pp. 109-116. Paris: sFi. uriforms (Loricariidae, Callichthyidae, Doradidae). Ann. Sci.
Nat.-Zool. Biol. Anim., 14(3): 101-123.
MeunieR F.J., DutHeiL D. & BRitO P.M., 2013. - Histological
study of the median lingual dental plate of the Cretaceous fish siRe J.y., GÉRAuDie J., MeunieR F.J. & ZyLBeRBeRG L.,
Palaeonotopterus greenwoodi (teleostei: Osteoglossomorpha) 1987. - On the origin of ganoine: Histological and ultrastruc-
from the Kem-Kem beds, Morocco. Cybium, 37(1-2): 121-125. tural data on the experimental regeneration of the scales of
Calamoichthys calabaricus (Osteichthyes, Brachyopterygii,
MeunieR F.J., MOnDeJAR-FeRnAnDeZ J., GOussARD F., Polypteridae). Am. J. Anat., 180: 391-402.
CLeMent G. & HeRBin, M., 2015a. - Presence of pliciden-
siRe J.y., DAVit-BeAL t., DeLGADO s., VAn DeR HeyDen
tine in the oral teeth of the coelacanth Latimeria chalumnae
C. & Huysseune A., 2002. - First-generation teeth in non-
smith 1939 (sarcopterygii; Actinistia). J. Struct. Biol., 190(1):
mammalian lineages: evidence for a conserved ancestral char-
31-37.
acter? Microsc. Res. Tech., 59: 408-434.
MeunieR F.J., De MAyRinCK D. & BRitO P.M., 2015b. -
stOCK D.W., 2001. - the genetic basis of modularity in the devel-
Presence of plicidentine in the labial teeth of Hoplias aimara
opment and evolution of the vertebrate dentition. Phil. Trans.
(erythrinidae; Ostariophysi; teleostei). Acta Zool., 96(2): 174-
R. Soc. Lond. B, 356: 1633-1653.
180.
STOCK D.W., 2007. - Zebrafish dentition in comparative context.
OWen R., 1840-1845. - Odontography. 655 p. London: H. Bail-
J. Exp. Zool. (Mol. Dev. Evol.), 308B: 523-549.
lère.
stReeLMAn J.t. & ALBeRtsOn R.C., 2006. - evolution of
PARADis M.R., RAJ M.t. & BOuGHneR J.C., 2013. - Jaw
novelty in the cichlid dentition. J. Exp. Zool. (Mol. Dev. Evol.),
growth in the absence of teeth: the developmental morphology
306B: 216-226.
of edentulous mandibles using the p63 mouse mutant. Evol.
Dev., 15(4): 268-279. stReeLMAn J.t., WeBB J.F., ALBeRtsOn R.C. & KOCHeR
t.D., 2003. - the cusp of evolution and development: a model
PAsCO-VieL e., CHARLes C., CHeVRet P., seMOn M., tAF-
of cichlid tooth shape diversity. Evol. Dev., 5: 600-608.
FOReAu P., ViRiOt L. & LAuDet V., 2010. - evolutionary
trends of the pharyngeal dentition in Cypriniformes (Actinop- stReeLMAn J.t., ALBeRtsOn R.C. & KOCHeR t.D., 2007. -
terygii: Ostariophysi). PLoS ONE, 5(6): e11293. Variation in body size and trophic morphology within and
among genetically differentiated populations of the cichlid fish,
PAsCO-VieL e., yAnG L., VeRAn M., BALteR V., MAyDen
Metriaclima zebra, from Lake Malawi. Freshw. Biol., 52: 525-
R.L., LAuDet V. & ViRiOt L., 2014. - stability versus diver-
538.
sity of the dentition during evolutionary radiation in cyprinine
stReit R.P., HOey A.s. & BeLLWOOD D.R., 2015. - Feeding
fish. Proc. R. Soc. B, 281: 2013-2688.
characteristics reveal functional distinctions among browsing
PeyeR B., 1968. - Comparative Odontology. 347 p. Chicago: herbivorous fishes on coral reefs. Coral Reefs, 34: 1037-1047.
univ. Press.
tRAPAni J., 2001. - Position of developing replacement teeth in
PLiKus M.V., ZeiCHneR-DAViD M., MAyeR J.A., ReynA J., teleosts. Copeia 1: 35-51.
BRinGAs P., tHeWissen J.G.M., sneAD M.L., CHAi y.
tRAPAni J., yAMAMOtO y. & stOCK D.W., 2005. - Ontoge-
& CHuOnG C.M., 2005. - Morphoregulation of teeth: modu-
netic transition from unicuspid to multicuspid oral dentition in
lating the number, size, shape and differentiation by tuning
a teleost fish: Astyanax mexicanus, the Mexican tetra (Ostario-
Bmp activity. Evol. Dev., 7(5): 440-457.
physi: Characidae). Zool. J. Linn. Soc., 145: 523-538.
RiCHMAn J.M. & HAnDRiGAn G.R., 2011. - Reptilian tooth
tuCKeR A.s. & FRAseR G.J., 2014. - evolution and develop-
development. Genesis, 49: 247-260.
mental diversity of tooth regeneration. Semin. Cell Dev. Biol.,
RÜBeR L., VeRHeyen e. & MeyeR A., 1999. - Replicated 25-26: 71-80.
evolution of trophic specializations in an endemic cichlid fish
tuCKeR A.s., HeADOn D.J., COuRtney J.M., OVeRBeeK
lineage from Lake tanganyika. PNAS USA, 96: 10230-10235.
P. & sHARPe P.t., 2004. - the activation level of the tnF
RÜCKLin M., DOnOGHue P.C.J., JOHAnsOn Z., tRinAJs- family receptor, edar, determines cusp number and tooth
tiC K., MAROne F. & stAMPAnOni M., 2012. - Develop- number during tooth development. Dev. Biol., 268: 185-194.
ment of teeth and jaws in the earliest jawed vertebrates. Nature,
VAnDeRVennet e., WAutieR K., VeRHeyen e. & Huys-
491: 748-751.
seune A., 2006. - From conical to spatulate: intra- and inter-
sCHiLLinG t.F., PiOtROWsKi t., GRAnDeL H. et al. [19 specific changes in tooth shape in closely related eretmodine
authors], 1996. - Jaw and branchial arch mutants in zebrafish. I. cichlids (teleostei; Cichlidae: eretmodini). J. Morphol., 267:
Branchial arches. Development, 123: 329-344. 516-525.
26 Cybium 2018, 42(1)
Huysseune & Witten Tooth shape in teleosts
WAutieR K., VAn DeR HeyDen C. & Huysseune A., 2001. Witten P.e. & HALL B.K., 2015. - teleost skeletal plasticity:
- A quantitative analysis of pharyngeal tooth shape in the Modulation, adaptation, and remodelling. Copeia, 103(4): 727-
zebrafish (Danio rerio, teleostei, Cyprinidae). Arch. Oral Biol., 739.
46: 67-75. ZAHRADniCeK O., BuCHtOVA M., DOseDeLOVA H. &
WAutieR K., Huysseune A. & VeRHeyen e., 2002. - tooth tuCKeR A.s., 2014. - the development of complex tooth
shape differences analyzed by biometric and morphometric shape in reptiles. Front. Physiol., 5: 74.
approaches: A case study on two morphologically very similar
lacustrine cichlid species. Conn. Tiss. Res., 43: 103-108.
Wise s.B. & stOCK D.W., 2010. - bmp2b and bmp4 are dispen-
sable for zebrafish tooth development. Dev. Dyn., 239: 2534-
2546.
Cybium 2018, 42(1) 27