review evolutionary and developmental origins of the ...jysire.free.fr/pdf/pdf...

J. Anat.

(2009)

214

, pp465–476 doi: 10.1111/j.1469-7580.2009.01053.x

© 2009 The Authors Journal compilation © 2009 Anatomical Society of Great Britain and Ireland

Blackwell Publishing Ltd

REVIEW

Evolutionary and developmental origins of the vertebrate dentition

Ann Huysseune,

1

Jean-Yves Sire

2

and P. Eckhard Witten

1

1

Biology Department, Ghent University, Belgium

2

UMR7138, Université Pierre et Marie Curie-Paris 6, France

Abstract

According to the classical theory, teeth derive from odontodes that invaded the oral cavity in conjunction with theorigin of jaws (the ‘outside in’ theory). A recent alternative hypothesis suggests that teeth evolved prior to theorigin of jaws as endodermal derivatives (the ‘inside out’ hypothesis). We compare the two theories in the light ofcurrent data and propose a third scenario, a revised ‘outside in’ hypothesis. We suggest that teeth may have arisenbefore the origin of jaws, as a result of competent, odontode-forming ectoderm invading the oropharyngeal cavitythrough the mouth as well as through the gill slits, interacting with neural crest-derived mesenchyme. This hypothesisrevives the homology between skin denticles (odontodes) and teeth. Our hypothesis is based on (1) the assumptionthat endoderm alone, together with neural crest, cannot form teeth; (2) the observation that pharyngeal teeth arepresent only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapodsconcomitant with the closure of gill slits, and (3) the observation that the dental lamina (

sensu

Reif, 1982) is not aprerequisite for teeth to form. We next discuss the progress that has been made to understand the spatiallyrestricted loss of teeth from certain arches, and the many questions that remain regarding the ontogenetic loss ofteeth in specific taxa. The recent advances that have been made in our knowledge on the molecular control oftooth formation in non-mammalians (mostly in some teleost model species) will undoubtedly contribute to answeringthese questions in the coming years.

Key words

dentition; development; evolution; odontodes; teeth; vertebrates.

Introduction

Teeth are elements of the dermal skeleton present in awide range of, typically, jawed vertebrates (Reif, 1982;Smith & Hall, 1990; Donoghue & Sansom, 2002). Owing totheir excellent preservation in the fossil record, the im-portant evolutionary information they contain and theirparadigmal status in developmental research, manypaleontological and neontological disciplines focus on teeth.Therefore it is not surprising that a number of excellenttextbooks and review articles have been devoted to thedevelopment and evolution of the vertebrate dentition.Hallmarks amongst these are Owen’s (1845) and Peyer’s(1968) seminal works, and the volumes edited by Miles(1967) and Teaford et al. (2000). Excellent reviews havebeen published in recent years on the development andevolution of the dentition in some selected lineages [see,

for example, Stock, 2007 on the dentition of zebrafish(

Danio rerio

) and its relatives; Davit-Béal et al. 2007 on theamphibian dentition; and Thenius, 1989 on mammaliandentitions]. However, large gaps still persist in the literatureregarding the development and evolution of actinoptery-gian and squamate dentitions.

Over the last 10 years, and since our previous review onthe subject (Huysseune & Sire, 1998), new ideas have beenadvanced and intriguing new data have been gatheredon the evolutionary history of the dentition. The focus ofthis paper is the evolutionary origin of teeth and theevolutionary modifications in the distribution of teeth, withemphasis on non-mammalian dentitions (developmentalaspects of the mammalian dentition being dealt with byCatón & Tucker, 2009).

Theories on the evolutionary origin of teeth

The ‘outside in’ theory

Where and when did teeth arise? According to the classicaltheory, teeth are derived from skin odontodes (dermaldenticles) that came to reside within the oral cavity when

Correspondence

A. Huysseune, Biology Department, Ledeganckstraat 35, B-9000 Ghent, Belgium. T: 32.9.264.52.29; F: 32.9.264.53.44; E: [email protected]

Accepted for publication

11 December 2008

Evo-devo of teeth, A. Huysseune et al.

© 2009 The AuthorsJournal compilation © 2009 Anatomical Society of Great Britain and Ireland

466

competent odontode-forming cells invaded the latter inconjunction with the origin of jaws (e.g. Ørvig, 1967;Peyer, 1968; Kemp, 1999), or even after the mandibulararch evolved (Reif, 1982). Ideas about the homology ofodontodes and teeth are based on paleontological evidence,the structural similarities of teeth and odontodes, and onthe shared developmental pathways of these elements(Huysseune & Sire, 1998). Both teeth and odontodes arecomposed of a dentin cone with a base of acellular or cellularbone-like tissue. In most cases the dentin is covered by ahypermineralized layer consisting of enamel or enameloid(Reif, 1982). Both structures have a pulp cavity that con-tains odontoblasts, connective tissue, nerve fibres andblood vessels. Extant chondrichthyans (sharks and rays)have retained odontodes, called placoid scales (Reif, 1982).Accordingly, shark teeth and shark placoid scales oftenserve as a textbook example illustrating the homologybetween these two elements (Huysseune & Sire, 1998; Hall& Witten, 2007).

The ‘inside out’ hypothesis

A recent, alternative hypothesis suggests that teethevolved prior to the origin of jaws, with oral teeth beingco-opted from endodermally derived pharyngeal denticles(the ‘inside out’ hypothesis, to distinguish it from the abovedescribed classical, ‘outside in’ theory). This hypothesis,with M.M. Smith and M. Coates as major proponents(Smith & Coates, 1998, 2000, 2001; Smith, 2003; Johanson& Smith, 2005), is based on both a reinterpretation of thefossil record and on embryological studies of extant species.First, Conodonta were accepted by Smith and co-workersto represent the first vertebrate group to show skeletalmineralisation, and conodont elements were seen as theearliest expression of oropharyngeal denticles (Smith &Coates, 1998). Second, the discovery of pharyngeal denticles,which showed a particular spiral arrangement, calledtooth whorls, in some thelodonts, agnathans (= jawlessvertebrates) found in 425 million year (Ma) old Siluriandeposits (Van der Brugghen & Janvier, 1993), was seen asimportant evidence that teeth were present in the pharynxprior to the establishment of jaws. In the view of Smith &Coates (2001), the arrangement of these whorl-like sets ofpharyngeal denticles suggests the presence of a dentallamina, considered by Reif (1982) to be the quintessentialcharacter of teeth and the only feature that could dis-tinguish teeth from odontodes. Smith & Coates (2001) pro-posed that these pharyngeal denticle whorl sets presagedthe polarised denticle whorl-like sets spaced around thejaw margin in primitive fossil and extant gnathostomes.Further support for their hypothesis was seen in the ideathat the splanchnocranium (to which pharyngeal denticlesare attached) should be considered different in originfrom the integumentary skeleton (and skin denticles) (cf.Donoghue & Sansom, 2002). It is worth noting however,

that in addition to pharyngeal denticles, thelodonts alsopossess an integumentary skeleton characterized bynumerous, minute odontodes similar to chondrichthyanodontodes (Janvier, 1996; Sire et al. 2009).

Additional arguments for the ‘inside out’ hypothesiswere also drawn from neontological research. The geneticindependence of tooth and jaw (and other dentigerousbone) development, required to support the independentorigin of the dentition from skin denticles, is supported bymany functional studies, mostly in mice (reviewed byMcCollum & Sharpe, 2001). Amongst teleosts, the so-called‘flathead’ mutants of the zebrafish (

Danio rerio

), a widelyused model species, reveal that teeth can develop in theabsence of the underlying branchial arch cartilage (Schillinget al. 1996). Essential for the ‘inside out’ hypothesis is thenotion that pharyngeal denticles develop in, and arepatterned by, endoderm (in conjunction with odontogenic,neural crest-derived mesenchyme). In zebrafish, thepresence and position of teeth on the last branchial archhas led to the widespread acceptance that pharyngealteeth develop from endodermal epithelium. This was seenas an argument in support of the ‘inside out’ hypothesis.

The evolutionary origin of jaw teeth from prepatterned,endodermally derived pharyngeal denticles, as suggestedby Smith & Coates (1998, 2000, 2001) and Smith & Johanson(2003a), has in turn been questioned by various authors onthe basis of paleontological data (Purnell, 2001; Milleret al. 2003; Burrow, 2003; Young, 2003). These argumentshave reciprocally been addressed by Smith & Johanson(2003b) and by Johanson & Smith (2005). In return, Hall(2005), and Reif (2002, 2006) have again argued in favourof the classical ‘outside in’ theory. Clearly, the debate isongoing.

A modified ‘outside in’ hypothesis

Here, we propose an alternative hypothesis that inte-grates both paleontological and embryological data, andis consistent with the above described findings. Weremove, however, the conodonts from the discussiongiven that only the Euconodonta are currently recognizedas vertebrates, yet that there is still no consensus about thestructural homology of their denticles with any kind ofvertebrate odontode (Scott, 1934; Morris, 1980; Pridmoreet al. 1996; Kemp, 2002a,b; Zhuravlev, 2005; Reif, 2006;Trotter et al. 2007; Janvier, 2007). In accordance with theclassic ‘outside in’ theory, we hypothesize that teeth arederived from odontodes, which were originally ectodermalin origin. These ectodermal odontodes developed insidethe oropharyngeal cavity as a result of competent ectodermmigrating inwards – not only via the mouth, but also viaeach of the gill slits (Fig. 1). Our hypothesis agrees with the‘inside out’ hypothesis in that we acknowledge that teethlikely arose prior to the origin of jaws [but the way jawsoriginated is itself seriously debated, as excellently



467

summarized by Janvier, 2007]. The odontogenic potentialof the ectodermal epithelium may have been subsequentlytransferred to the endoderm, provided there was anintimate contact between these two germ layers, such aswhere mouth and gill slits form. Consequently, providedpharyngeal denticles or teeth indeed develop from endo-dermal epithelium, the adjacent presence or even physicalcontact of ectoderm with endodermal epithelium wouldhave been a requirement for their development. Yet, un-equivocal evidence for an endodermal origin of pharyngealteeth or denticles in extant primitive gnathostomes,and by inference in extinct thelodonts, still needs to becollected. Although widely accepted based on position inthe endodermal lining of the pharynx (see, for example,Piotrowski & Nüsslein-Volhard, 2000; Yelick & Shilling,2002), unequivocal evidence supporting the endodermalorigin of pharyngeal teeth remains wanting as universal,reliable markers of endoderm are at present unavailable.Using clonal analysis, it has been shown that in the zebrafishthe pharyngeal epithelium is only partially derived fromendoderm (Warga & Nüsslein-Volhard, 1999). To date,strong evidence for endodermal participation in toothformation has been collected only for urodele amphibians.However, careful examination of the reports of the manyexperimental studies that have been carried out onsalamanders in the last century, indicates that ectodermand endoderm are both required to form teeth (e.g. Ströer,1933; Sellman, 1946; Wilde, 1955), or, if teeth developfrom supposedly endodermally derived enamel organs,the ectoderm is required (Sellman, 1946) or at the very leastit was not removed (e.g. Adams, 1924; de Beer, 1947; Barlow& Northcutt, 1995). Only Cassin & Capuron (1979) reportteeth forming in grafts with neural crest and endodermalone. Working with

Pleurodeles waltl

, Chibon (1966,1970), on the other hand, noted that the odontoblasts

exert an inductive action upon the epithelium, which canbe an ectodermal epithelium (in anterior teeth), an endo-dermal epithelium (in posterior teeth), or one of mixedorigin. A recent study on the axolotl (

Ambystoma mexicanum

)using GFP transgenes has confirmed Chibon’s hypothesisthat the epithelial component of the teeth can be bothectodermal and endodermal (Soukup et al. 2008). Never-theless, the experiments of Soukup et al. (2008) do notrepresent evidence against the necessity of a close proximitybetween ectoderm and endoderm. In these experiments,it remains to be clarified whether the participation ofendoderm in the enamel organs is not just an expressionof a potential not normally displayed during regulardevelopment, rather than the normal

in vivo

capacity.Other not normally odontogenic tissues have indeed beenshown to be able to express an odontogenic potential. Forexample, using the same species (

A. mexicanum

), Gravesonet al. (1997) demonstrated that caudal regions of neuralcrest cells, not typically involved in tooth formation duringnormal development, can produce teeth under the appro-priate

in vitro

conditions. Graveson et al. (

op. cit.

) attributedthis unexpressed potential to an apparent lack of exposureof these neural crest cells to the appropriate inductivetissues, i.e. stomodeal ectoderm and oral endoderm(Sellman, 1946; Wilde, 1955; Graveson, 1993). Graveson’sexperiments were nevertheless not a test of whether teethform from endodermal or ectodermal epithelium. Amongmammals, Imai et al. (1998) used an endodermal cell-tracing system with a recombinant adenovirus, but couldonly demonstrate that tooth germs in the rat form inectoderm

adjacent

to labelled endodermal cells (foregutendoderm); they did not find evidence for an active role ofthe endoderm itself. Returning to zebrafish teeth, it israther confusing that, on the one hand, Smith & Coates(1998) use the argument of zebrafish mutants to show

Fig. 1 Comparison of the arrangement of the gill slits, the position of the branchial arches and of the gills in agnathans (A) and gnathostomes (B,C). Odontodes and dermal bones are indicated in red. (A,B) Extent of ectoderm (blue) and endoderm (yellow) as usually assumed. In (C) we postulate (contra B) that the ectoderm penetrates further inwards (arrowheads), and possibly covers the endoderm, as observed by Edwards (1929) (cf. Fig. 3) (modified after Jollie, 1968).



468

that teeth can develop independently from the underlyingsplanchnoskeleton, and, on the other hand, link teeth andsplanchnoskeleton in emphasizing the need for endodermto pattern both. Johanson & Smith (2005, p. 339) expressthis as ‘this regulatory mechanism from endoderm can alsobe utilised for denticles and teeth as part of the splanch-nocranial skeleton’.

The key issue of our revised hypothesis is the assumptionthat odontogenic competent ectoderm invaded theoropharyngeal cavity through both the mouth and the gillslits. Even if odontogenic competence would have beentransferred from ectoderm to endoderm (i.e. the tooth-forming capacity would have come to reside in theendoderm – an assumption that still needs to be tested inrepresentative species of basal actinopterygian lineages,e.g. polypterids, the bichirs), tooth-forming endodermwould still require a close proximity, perhaps even physicalcontact, with the ectoderm.

Paleontological data can be reconciled with this view aslong as it can be shown that the taxa known to possesspharyngeal denticles possessed gill slits, or other structurespermitting ectoderm to penetrate into the body, such asthe nasopharyngeal duct (including Rathke’s pouch) or thespiraculum (corresponding to the opening between man-dibular and hyoid arch) (cf. Bjerring, 1977).The denticles inthe thelodont

Loganellia

extend anteriorly onto thewall of the large median nasopharyngeal duct (Van derBrugghen & Janvier, 1993). One may thus assume that theycould develop because of an ectodermal contributionthrough this duct. Most osteostracans have slit-shapedexternal gill openings, the condition in tremataspidids (withsmall rounded openings) being derived; extant agnathans(hagfish and lampreys) and most extinct agnathans(anaspids, astrapidids and galeaspids) have small rounded-shaped external gill openings (Janvier, 2007, p. 92). However,even the possession of reiterative slits is not a require-ment, as physical contact between ectoderm and endoderm,without the formation of an open gill slit proper, could besufficient for interactions to occur between the two tissuelayers. In the zebrafish, the first tooth anlage appears aftera connection has been established between ectodermand endoderm in the form of an elongate, initially two-cell-thick strand bridging the skin with the pharynx onboth sides, well before the actual formation of the gill slitwithin this strand (Fig. 2). Interestingly, Jackman et al.(2004) found that treatment of 32–78-h zebrafish embryoswith SU5402 (a lipophilic reagent, which inhibits signalingthrough inactivation of FGF receptors) affected both earlydental epithelial morphogenesis and 6th pharyngealpouch morphology. In our view, the altered toothmorphogenesis likely results from an altered signalingfrom the pouch epithelium. In 1929, Edwards performed adetailed embryological study of mouth and pharynxformation in the carp (

Cyprinus carpio

), a family member ofthe zebrafish that also forms pharyngeal teeth. By careful

analysis of histological sections, he concluded that in thetooth-forming region, the pharyngeal epithelium wascomposed of a superficial layer of flattened cells, derivedfrom migration of ectoderm, overlying a layer of endodermalepithelium. Edwards (1929) also reported that the enamelorgans were derived from the deep (endodermal) layer,but clearly illustrated the close contact between ectodermaland endodermal layers (Fig. 3).

According to Smith & Coates (1998), differences inpatterning and regulation of pharyngeal denticles (whencompared to odontodes), and the putative presence of adental lamina, provide supporting evidence for their‘inside out’ hypothesis. Upon closer investigation, we viewthese interpretations as doubtful based on the following:(1) Teeth (pharyngeal or associated to other parts of thevisceral skeleton) often display a highly unordered patternin extant species [e.g. on the pharyngeal jaws of cichlids(Huysseune, 1995), the oral jaws of gadids (Holmbakken &Fosse, 1973), or during certain life stages of the fish, suchas the post-spawning period in wild Atlantic salmon (Wittenet al. 2005)]. Also, whereas differential gene expressionpatterns in oral vs. pharyngeal teeth in rainbow trout havebeen used to support the suggestion that oral teethevolved by co-option from pharyngeal teeth (Fraser et al.2004), gene expression data from medaka (

Oryzias latipes

)support the notion of serial homology between oral andpharyngeal teeth (Debiais-Thibaud et al. 2007). In ourview there is no proof for germ layer-related fundamental

Fig. 2 Semithin sections of forming pharyngeal pouches in zebrafish (Danio rerio) at 56 h (A) and 72 h (B) post-fertilization. (A) An epithelial connection (black arrowheads) is seen between the epidermis (white asterisks) and the foregut (black asterisk). (B) The first tooth germs (white arrowhead) are forming whilst the gill slits are still closed (black arrowheads), and the pharyngeal lumen opens (black asterisk). Scale bars = 40 μm.



469

developmental differences between teeth and odontodes.(2) Teeth can form without a dental lamina (Fig. 4A). Thereare many examples of jaw teeth forming without passingthrough a dental lamina stage (see, for example, Donoghue& Aldridge, 2001, for such examples). In addition, first-generation teeth, widely considered to be representativeof an ancestral type of teeth, develop from the superficialepithelium in most non-mammalian osteichthyans exam-ined so far (Sire et al. 2002). Furthermore, not even a dis-continuous and non-permanent dental lamina (

sensu

Reif,1982) is required for tooth replacement, as demonstrated

for salmon by Huysseune & Witten (2008) (compare Fig. 4Awith 4B–F). (3) Short whorl-like arrangements of teeth canbe produced without a dental lamina. In zebrafish, thefirst tooth generations in position 4V are co-functional(Van der heyden & Huysseune, 2000). These teeth form aseries with a whorl-like arrangement due only to spaceconstraints. A successional lamina is virtually non-existentin these early tooth generations; it only becomes prominentat older developmental stages (Huysseune, 2006). Finally,one should also consider the possibility that patterning ofpharyngeal denticles into families (as exemplified inthelodonts) may well be the outcome of a heterochronicshift of patterning of the crowns of skin denticles. Mergingof pharyngeal denticles into a single unit would yield asingle crown with a herring bone-like morphology com-parable to that of skin denticles. It is worth noting that theearliest chondrichthyan teeth are of ‘diplodont’ type (i.e.having a base bearing two large divergent cusps, and oneor two smaller cusps in-between) (Janvier, 1996, p. 149).Interestingly, this tooth morphology is similar to that ofmost pharyngeal denticles in basal chondrichthyans andosteichthyans.

The presence of teeth in the pharyngeal cavity couldthus have been an early event in vertebrate evolutionwhereby ectoderm invaded through the gill slits, possiblyinteracting with endoderm, thereby being involved inpharyngeal denticle (teeth) development. One obviousquestion to ask is why pharyngeal teeth did not evolvemore often? Denticles cover the median part of the oralroof in some osteostracans, which, together with thelodonts,are the only agnathans with oral or pharyngeal denticles(Janvier, 2007). The relative rarity of pharyngeal denticles inagnathans may be related to differences in the distributionof ectoderm and endoderm at the gill slits, as evidenced bythe differing origins of gill filaments in modern lampreysand gnathostomes. Early in the 20th century it was dis-covered that lamprey gill filaments are endodermal in origin,and, alongside the branchial nerves and blood vessels,reside medial to the skeletal gill arches (Goette, 1901). Incontrast, among gnathostomes, gill filaments are ecto-dermal in origin and, at least in osteichthyans, are positionedlateral to the skeletal gill arches (Goette, 1901; Janvier,2007). If ectoderm penetrated also less deeply into thegill slits in extinct agnathans, or only late, this could be areason why pharyngeal denticles are not more widespreadin agnathans.

Our hypothesis states that teeth originated prior tojaws, but only when the formation of gill slits allowed fora relatively deep invasion of ectoderm into the oropharyngealcavity and extensive physical contact between ectodermand endoderm. Such a scenario may explain why pharyngealteeth, located deeply within the oropharyngeal cavity,were lost in early tetrapods and maintained only on themargins of the jaws and roof of the oral cavity. We pro-pose that loss of gill slits, and the ability for the ectoderm

Fig. 3 Three stages in the development of the gill slits and pharynx of the carp (Cyprinus carpio). (A–C) respectively 36, 56 and 78 h post-fertilization. An ectodermal plug (blue) invaginates the endodermal pharyngeal folds (yellow) (A) and forms a layer of flattened (ectoderm-derived) cells (blue) on top of the columnar (endoderm-derived) epithelial cells (yellow) (B,C). The latter produce the enamel organs of the teeth. 4v, fourth ventricle; Br, brain; Ep, proliferating ectodermal plug; Es, epidermal stratum; Ga, gill arch; Gs, gill slit; Ha, hyoid arch; Nl, inner layer of ectoderm; No, notochord; Ov, otic vesicle; Pf, pharyngeal fold (modified after Edwards, 1929).



470

to invade, leads to the disconnection of the competentectodermal epithelium and the endodermally linedpharynx. Data gleaned from the fossil record supports thisconclusion. For example, among Tetrapodomorph fish,the group of lobe-finned fish (sarcopterygians) that isgenerally believed to have given rise to tetrapods, with

Eusthenopteron

(late Devonian, 385 Ma) as an importantrepresentative, the internal surfaces of the gill arch ele-ments are covered with tooth plates (Nelson, 1969; Carroll,1988). The branchial skeleton of

Ichthyostega

, an upperDevonian (365 Ma) amphibian close to the ancestry of alllater terrestrial vertebrates, is poorly known, but the animalpossibly had a small gill slit (Janvier, 1996).

Acanthostega

,an early tetrapod from the upper Devonian, retained afish-like branchial skeleton, fish-like internal gills and anopen opercular chamber for use in aquatic respiration(Coates & Clack, 1991), and it possessed branchial toothplates (Coates, 1996 in Graveson et al. 1997).

Acanthostega

falls outside the Neotetrapoda, a group that is characterizedby the closure of the gill slit (Janvier, 1996). Branchial toothplates have also been reported for the basal temnospondylamphibian

Colosteus scutellatus

(upper Carboniferous,310 Ma) (Hook, 1983). Interestingly, Schoch (2002) notedthe coincidence between the loss of branchial denticles,considered to be homologous to teeth, and the loss of gillslits in temnospondyls (Fig. 5). Schoch (2002) suggested afunctional explanation for the simultaneous loss of bothbranchial denticles and gill slits: open gill clefts allow for aunidirectional flow of water from the buccal cavitythrough the branchial chamber, thus enabling branchial

denticles to assist in the capture and processing of preyitems. Paleontologists indeed tend to use the presence ofdenticulated pieces of bone (branchial ossicles,

sensu

Schoch, 2001) in temnospondyl amphibians as evidence forthe presence of a (cartilaginous) branchial skeleton (Boy,1988) and open gill slits (e.g. Berman, 1973; Schoch, 2001).We propose that the simultaneous loss of gill slits and ofpharyngeal denticles (teeth) is not just functionally butalso developmentally related, as the loss of gill slits couldprevent the invagination of odontogenic, or inductivelycompetent, ectoderm. However, it is important to notethat the presence of gill slits does not necessarily predictthe development of branchial denticles. For example,lungfish (Dipnoi) lack pharyngeal denticles. This is assumedto be a secondary loss, possibly related to the extensiveevolution of the dentition during the early history of thegroup (Ahlberg et al. 2006). The loss could be analogous tothe loss of teeth on the different gill arches in teleosts.

Also significant to our hypothesis is that in no othertetrapods have pharyngeal teeth, or branchial denticles,ever been observed, despite the presence of pharyngealendoderm, and despite the likely presence of segmentallyarranged ectodermal–endodermal contacts. We speculatethat such contacts are constituted solely of outpockets ofendoderm abutting the ectoderm, and that withoutectodermal invagination into the body, tooth developmentis not initiated. This will be easy to test once a reliablemarker for endoderm is available. In the urodele amphibian

Ambystoma mexicanum

, endodermally derived oral teethare formed in close proximity to the invaginated ectoderm

Fig. 4 Different types of dental lamina (black arrowheads) during tooth replacement. Replacement tooth formation without the presence of a dental lamina (A, Atlantic salmon, Salmo salar); with a transient, successional dental lamina (B, zebrafish, Danio rerio, and C, jewel cichlid, Hemichromis bimaculatus), or with a permanent dental lamina (D, Pleurodeles waltl, a urodele amphibian; E, Chalcides sexlineatus, a scincid lizard; F, human first lower deciduous molar). boa, bone of attachment; db, dentigerous bone; dp, dental papilla; eo, enamel organ; oe, oral epithelium; pe, pharyngeal epithelium; t, tooth. Scale bars (A–E) = 50 μm, (F) = 500 μm. (F), courtesy of Ralf J. Radlanski.



471

(Soukup et al. 2008). In our view, the concomitant lack ofgill slits and pharyngeal teeth in tetrapods is a strongargument for the ectodermal origin of teeth. Even if thecompetence to form teeth had been transferred duringevolution from ectoderm to endoderm, and the ectodermwould still be required as an inductive tissue, tooth for-mation would be blocked because of the loss of extensivecontact between the two embryonic layers (ectoderm andendoderm).

Given that the spiraculum, similar to other gill slits,could allow ectoderm to migrate inwards, it is interestingto note that

Eusthenopteron

retains denticles inside thespiracular canal (Jarvik, 1980). Most tetrapod stem groupmembers are now assumed to retain an open spiraculum(Clack, 2007). Possibly, the rise of the tympanic membranecould have been the ultimate event that definitivelysealed off this route for ectodermal migration.

The recent discussion in the literature of whetherplacoderms (e.g. antiarchs, arthrodires), phylogeneticallythe most basal clade of jawed vertebrates (early Silurian tolate Devonian, 435–360 Ma), have pharyngeal denticles,can also be viewed in the light of our proposed hypothesis.The so-called postbranchial lamina, which carries patternedarrays of denticles (Johanson & Smith, 2003, 2005) is againan area where invagination could have carried ectodermalcompetence deep into the body. Johanson & Smith (2005)

saw a difference in arrangement and morphology betweenthese organized denticles and those ornamenting thesurface of the head shield. Again, for the reasons givenabove, we do not consider differences in patterningsufficient to justify an independent, endodermal origin ofpharyngeal denticles. In the case of the placoderm post-branchial lamina, the pharyngeal denticles may representanother ‘experiment’ of nature. We consider them ‘experi-ments’ as much as we, and others, consider extra-oral teeth(see below) a developmental ‘experiment’ the other wayaround (inwards out, i.e. production of structures outsidethe mouth by a developmental programme used normallyto produce structures inside the oral cavity only). Thisinterpretation implies that the occurrence of pharyngealdenticles in agnathans and early gnathostomes holds nophylogenetic information, and hence avoids discussionsand speculations on the multiple origins of teeth throughconvergent evolution (Smith & Johanson, 2003a).

Our hypothesis revives the view of Nelson (1969, 1970),who assumed that small tooth plates were distributedover the entire surface of the oropharyngeal cavity early ingnathostome evolution, comparable to the distribution ofplacoid scales in elasmobranchs (cf. Reif, 1982), and thatthese tooth plates, whether large or small, were freelylocated in the tissues. Subsequently, enlarged tooth platesmay have appeared in areas of particular functionalimportance, and possibly first on the jaws. AlthoughNelson did not explicitly state that competent ectodermentered the oropharyngeal cavity through the gill slits, hedoes refer to a relation between the presence (or absence)of gill slits and the presence (or absence) of tooth plates.

Evolutionary modifications in the distribution of teeth

A prominent evolutionary trend towards tooth reduction

Looking at the distribution of teeth both in actinopterygianand sarcopterygian lineages, it is clear that the number oftooth-bearing skeletal elements has been reduced duringvertebrate evolution. An overview of these trends waspresented by Huysseune & Sire (1998). Among sarcoptery-gians,

Latimeria

has many dental plates associated withthe jaws, palatal bones, hyoid and branchial arches (Millot& Anthony, 1958). The dentition associated with the(post-hyoid) visceral arches was lost in early tetrapods, aloss formerly associated with the loss of respiratory functionin the transition from aquatic to terrestrial life. We nowbelieve that loss of the dentition on the visceral arches isonly secondarily associated with the loss of their respiratoryfunction and primarily associated with the loss of thegill slits (see above). In caudate lissamphibians, larval teethare attached to the paired bones of the upper jaw (pre-maxillaries, maxillaries, prevomers and palatines) and the

Fig. 5 Branchial denticulated plates (branchial ossicles) in the pre-metamorphosis stage of Onchiodon labyrinthicus, a temnospondyl amphibian from the lower Permian (reproduced from Schoch, 2001, Fig. 3, with permission from the author).



472

lower jaw (dentaries and coronoids) (Davit-Béal et al. 2007).During metamorphosis, the palatines disappear fromthe upper jaw and are replaced by the extension of thevomers. In the lower jaw, the coronoids disappear and onlythe dentaries remain. In anurans, teeth, when present, arerestricted to the upper jaw, with the exception of somehylids, in which teeth are also found on the dentary (seeDavit-Béal et al. 2007, for a review). Vomers, as well as theparasphenoid bone, are believed to be evolutionarilyderived from the anterior part of the splanchnocraniumtoo (Nelson, 1969; for a historical review and critical com-ments on the interpretation of the anterior neurocranialskeleton, see Kimmel & Eberhart, 2008). The restriction ofteeth to these skeletal elements can be easily explained bythe fact that an ectodermal-endodermal contact necessaryto allow these teeth to form, is established only throughthe mouth opening. By extension, this may explain therestricted oral distribution of teeth in sauropsids (Edmund,1969) and in mammals (Thenius, 1989).

Within the actinopterygians, the teleost fish, with26 000 species representing approximately one third of allextant vertebrate species, display a prominent evolutionarytrend in the loss of teeth from different visceral arches.Representatives of basal teleostean lineages such aselopomorphs have tooth plates associated with all branchialarches. In contrast, advanced teleosts, such as acantho-morphs, usually retain teeth only on the mandibular and theposteriormost branchial arches (Nelson, 1969; Vandewalleet al. 1994). In the ostariophysan lineage on the otherhand, oral teeth have been lost in cypriniforms (Stock,2007). Tooth loss in these teleost taxa can not, of course,be explained by a loss of ectodermal invagination andectodermal/endodermal interactions as all teleosts retaingill slits. Instead, the cause of tooth loss is more likely to befound in changes in the molecular networks that regulatetooth initiation, under the selective pressure of regionali-zation of functions with respect to food processing andrespiration.

Molecular networks regulating tooth formation in non-mammalians

We are only scratching the surface in our understanding ofthe molecular networks that are responsible for toothformation in non-mammalians, and there is an enormousbacklog in knowledge compared to what is known formammals (mostly in the mouse) (see the review by Catón& Tucker, 2009). However, at least one question that hasbeen settled over the past years is whether and how teethcan develop in a Hox-expressing environment, as is thecase for the post-mandibular arches in non-mammalians(Prince et al. 1998). Indeed, teeth in mammals develop onthe mandibular arch only, which is a non-Hox expressingenvironment (Rijli et al. 1993). It had previously beendemonstrated that, at least in birds, Hox-gene expression

and jaw formation are mutually exclusive (Couly et al.1998; Grammatopoulos et al. 2000). James et al. (2002)experimentally demonstrated that teeth in the mouse candevelop in a Hox-expressing environment. This impliesthat, whereas a loss of Hox gene expression in the firstbranchial arch might have been required for jaws to form(Rijli et al. 1993; Cohn, 2002), the evolutionary acquisition ofteeth on the first arch was independent of a Hox patterningprogramme.

The small number of papers published so far onexpression patterns of developmental genes involved intooth formation in non-mammalians have revealed bothconserved and divergent patterns when compared tomammals (Fraser et al. 2004, 2006a,b; Jackman et al. 2004;Laurenti et al. 2004; Borday-Birraux et al. 2006; Wise &Stock, 2006; Debiais-Thibaud et al. 2007; Huysseune et al.2008). A profound knowledge of the molecular networksand the genes involved is nevertheless imperative ifwe want to approach the question of ontogenetic andevolutionary tooth loss. To date, most of what is knownabout the evolutionary loss of teeth associated withcertain branchial arches has been published by Stock andcolleagues (Stock et al. 2006; Jackman & Stock, 2006; Wise& Stock, 2006; Stock, 2007). Briefly summarized, Stock andcolleagues first discovered that oral tooth loss in cyprini-forms is associated with a loss of oral

bmp2b

(Wise & Stock,2006) and oral

dlx2b

expression (Stock et al. 2006), twodevelopmental genes involved in tooth formation (Jackmanet al. 2004; Wise & Stock, 2006). Next, using a zebrafish

dlx2b

:GFP reporter construct, they showed that this con-struct can drive

dlx2b

expression in the oral tooth germsin a member of the sister lineage, the Mexican tetra(

Astyanax mexicanus

, a characiform), indicating that lossof oral

dlx2b

expression in cypriniforms results fromchanges in one or more

trans

-acting regulators ratherthan in the

cis

-regulatory regions of this gene (Jackman &Stock, 2006). These authors concluded that preservation oforal enhancer function, unused for more than 50 millionyears, could be the result of pleiotropic function in thepharyngeal dentition.

The above-mentioned findings raise the question ofwhether teeth can be re-acquired after having been lost incertain areas of the oropharyngeal cavity, or from certainbones. One example is the reappearance of the secondlower molar tooth in extant lynx (

Felis lynx

) (Kurtén, 1963).The reappearance of a fourth row of pharyngeal teeth inthe cyprinid fish

Barbus paludinosus

(Golubtsov et al. 2005)has been discussed as a possible case of taxic atavism. Similarto the spontaneous reappearance of lost characters inindividuals (atavism), lost characters can reappear in entiretaxa (taxic atavism) (Stiassny, 1991). Additional examplesof taxic atavisms from other taxa and other organ systems(fins, muscles, skull bones) are discussed by Raikow et al.(1979), Meyer (1999), Gatesy et al. (2003) and Hall (2007).Other studies relevant to the evolutionary loss of teeth in



473

tetrapods are reviewed by Davit-Béal et al. (2009) in thisvolume.

Spatially restricted tooth loss (such as the loss of oralteeth in cyprinids or tooth loss on the lower jaw in mostfrogs) or ontogenetic tooth loss [such as in sturgeons(Peyer, 1968), in armoured catfish (Huysseune & Sire, 1997),or in

Pangasianodon gigas

, the giant catfish (Kakizawa &Meenakarn, 2003)], reveals the presence of developmentalmodules in the dentition, as discussed by Stock (2001). Inan excellent review, this author analysed the variouslevels at which modules (units that develop under semi-autonomous control) can be identified in the vertebratedentition, and discussed how these could be related tomodularity in the genetic control of development.

The case of extra-oral teeth

A final issue regarding the distribution of teeth in theoropharyngeal cavity that needs to be addressed concernsa developmental conundrum, which is the presence ofextra-oral teeth. Within recent years, several teleost specieshave been described with denticles structurally identical toteeth, developed across extra-oral surfaces of the head.These species represent a wide diversity of unrelatedlineages including Siluriformes (Sire & Huysseune, 1996),Clupeomorpha (Sire et al. 1998), Atheriniformes (Sire &Allizard, 2001), Xiphioidea (Sire & Allizard, 2001) andLophiiformes (Pietsch & Orr, 2007). Initially, these extra-oralelements were considered to be dermal denticles reminiscentof ancestral odontodes (e.g. Sire & Huysseune, 1996).However, given the variety of species involved it becameclear that these structures should be regarded as a novelactivation of an existing tooth developmental programmein extra-oral locations and not merely as the reappearanceof an ancestral character (Sire, 2001, see also Stock, 2001).Note that such developmental ‘experiments’ have onlybeen reported for the ectoderm and not for the endoderm,lending support to the idea of an ectodermal primacy intooth evolutionary history.

Conclusions and perspectives

Based on a reappraisal of available evidence, we challengethe current views of the evolutionary origin of teeth, andpropose a revised ‘outside in’ hypothesis. We suggest thatteeth may have arisen before the origin of jaws, as a resultof the invasion of competent, odontode-forming ectoderminto the oropharyngeal cavity through the mouth and gillslits, to interact with neural crest-derived mesenchyme(Hall, 2000). This hypothesis supports the homology betweenskin denticles (odontodes) and teeth.

Our hypothesis is based on (1) the assumption thatendoderm alone, together with neural crest, cannot formteeth, given that – with one exception – supposedly endo-dermally derived teeth were never observed to develop

without the nearby presence of ectoderm in extant species;(2) the observation that pharyngeal teeth are present onlyin species known to possess gill slits, and disappear fromthe pharyngeal region in early tetrapods concomitantwith the closure of gill slits, and (3) the assumption thatthe dental lamina (

sensu

Reif, 1982) is not a prerequisitefor tooth development, although it may have facilitatedtooth formation in advance of need. We regard thepresence of pharyngeal denticles in extinct thelodonts,and the postbranchial lamina denticles of placoderms asindependent ‘experiments’ of nature, involving the sameodontogenetically competent tissues, that is, neural crest andectoderm. Extra-oral teeth observed in various unrelatedtaxa of teleost fishes, are seen as similar developmental‘accidents’, but the other way around, carrying the toothdevelopmental programme to the external surface of thebody. Whereas our revised ‘outside in’ hypothesis accountsfor the complete loss of teeth from the post-mandibularbranchial arches, it cannot explain the spatially restrictedloss of teeth from certain arches, as occurs in numerousteleosts and frogs, or the ontogenetic loss of teeth inspecific taxa.

One of the primary advantages of our hypothesis isthat it can be tested on paleontological data (it predicts acorrelation between the presence of pharyngeal teeth andgill slits) and developmental data in extant species (bychallenging endoderm alone to make teeth in associationwith neural crest-derived mesenchyme). In addition, it mayserve as a guide for further developmental research, suchas a search for an ectodermal signal necessary for pharyngealtooth development.

The recent advances that have been made in ourknowledge on the molecular control of tooth formation innon-mammalians (mostly in some teleost model species)will undoubtedly contribute to answering these questionsin the coming years.

Acknowledgements

The authors acknowledge the insightful comments of two anony-mous referees. This paper was made within the frame of the EuropeanCOST ACTION B23-Oral facial development and regeneration. A.H.acknowledges grants from the FWO-Vlaanderen nos 3G0159.05and KaN 1.5.116.06.

References

Adams AE

(1924) An experimental study of the development ofthe mouth in the amphibian embryo.

J Exp Zool

40

, 311–379.

Ahlberg PE, Smith MM, Johanson Z

(2006) Developmental plasticityand disparity in early dipnoan (lungfish) dentitions.

Evol Dev

8

,331–349.

Barlow LA, Northcutt RG

(1995) Embryonic origin of amphibiantaste buds.

Dev Biol

169

, 273–285.

Berman DS

(1973) A trimerorhachid amphibian from the upperPennsylvanian of New Mexico.

J Paleontol

47

, 932–945.



474

Bjerring HC

(1977) A contribution to structural analysis of the headof craniate animals.

Zool Scr

6

, 127–183.

Borday-Birraux V, Van der heyden C, Debiais-Thibaud M, et al.

(2006) Expression of

dlx

genes in zebrafish tooth development.Evolutionary implications.

Evol Dev

8

, 130–141.

Boy JA

(1988) Über einige Vertreter der Eryopoidea (Amphibia:Temnospondyli) aus dem europäischen Rotliegend (?höchstesKarbon-Perm). 1.

Sclerocephalus

.

Paläont Z

62

,107–132.

Burrow CJ

(2003) Comment on ‘Separate evolutionary origins ofteeth from evidence in fossil jawed vertebrates’.

Science

300

,1661b.

Carroll RL

(1988)

Vertebrate Paleontology and Evolution

. NewYork: W.H. Freeman & Company.

Cassin C, Capuron A

(1979) Buccal organogenesis in

Pleurodeleswaltl

Michah (urodele amphibian), study by intrablastocelictransplantation and

in vitro

culture.

J Biol Buccale

7

, 61–76.

Catón J, Tucker A

(2009) Current knowledge of tooth development,a model mineralized element system.

J Anat

214

, 502–515.

Chibon P

(1966) Analyse expérimentale de la régionalisation et descapacités morphogénétiques de la crête neurale chez l’amphibienurodèle

Pleurodeles waltlii

Michah.

Mém Soc Zool Fr

36

, 1–107.

Chibon P

(1970) L’origine de l’organe adamantin des dents. Etudeau moyen du marquage nucléaire de l’ectoderme stomodéal.

Ann Embryol Morphol

3, 203–243.Clack JA (2007) Devonian climate change, breathing and the origin

of the tetrapod stem group. Integr Comp Biol 47, 510–523.Coates M (1996) The Devonian tetrapod Acanthostega gunnari

Jarvik: postcranial anatomy, basal tetrapod interrelationships,and patterns of skeletal evolution. Trans R Soc Edin 87, 363–421.

Coates MI, Clack JA (1991) Fish-like gills and breathing in the earliestknown tetrapod. Nature 352, 234–236.

Cohn MJ (2002) Lamprey Hox genes and the origin of jaws. Nature416, 386–387.

Couly G, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM (1998)Determination of the identity of the derivatives of the cephalicneural crest: incompatibility between Hox gene expression andlower jaw development. Development 125, 3445–3459.

Davit-Béal T, Allizard F, Sire J-Y (2007) Enameloid/enamel transitionthrough successive tooth replacements in Pleurodeles waltl(Lissamphibia, Caudata). Cell Tissue Res 328, 167–183.

Davit-Béal T, Tucker A, Sire J-Y (2009) Loss of teeth and enamel intetrapods: Fossil record, genetic data and morphologicaladaptations. J Anat 214, 477–501.

de Beer GR (1947) The differentiation of neural crest cells intovisceral cartilages and odontoblasts in Amblystoma, and a re-examination of the germ-layer theory. Proc R Soc Lond B 134,377–398.

Debiais-Thibaud M, Borday-Birraux V, Germon I, et al. (2007)Development of oral and pharyngeal teeth in the medaka(Oryzias latipes): Comparison of morphology and expression ofeve1 gene. J Exp Zool 308B, 693–708.

Donoghue PCJ, Aldridge RJ (2001) Origin of a mineralized skeleton.In Major Events in Early Vertebrate Evolution (ed. Ahlberg PE),Systematics Association Special Volume Series 61, pp. 85–104.

Donoghue PCJ, Sansom IJ (2002) Origin and evolution of verte-brate skeletonization. Microsc Res Techn 59, 352–372.

Edmund AG (1969) Dentition. In Biology of the Reptilia. Vol. 1.Morphology A (eds Gans C, Bellairs Ad’A, Parsons TS), pp. 117–200. London: Academic Press.

Edwards LF (1929) The origin of the pharyngeal teeth of the carp(Cyprinus carpio Linnaeus). Ohio J Sci 29, 93–130.

Fraser GJ, Berkovitz BK, Graham A, Smith MM (2006b) Genedeployment for tooth replacement in the rainbow trout(Oncorhynchus mykiss): a developmental model for evolution ofthe osteichthyan dentition. Evol Dev 8, 446–457.

Fraser GJ, Graham A, Smith MM (2004) Conserved deployment ofgenes during odontogenesis across osteichthyans. Proc R SocLond B 271, 2311–2317.

Fraser GJ, Graham A, Smith MM (2006a) Developmental andevolutionary origins of the vertebrate dentition: molecular controlsfor spatio-temporal organisation of tooth sites in osteichthyans.J Exp Zool 306B, 183–203.

Gatesy J, Amato G, Norell M, DeSalle R, Hayashi C (2003) Combinedsupport for wholesale taxic atavism in gavialine crocodylians.Syst Biol 52, 403–422.

Goette A (1901) Über die Kiemen der Fische. Z Wissenschaftl Zool69, 533–577.

Golubtsov AS, Dzerjinskii KF, Prokofiev AM (2005) Four rows ofpharyngeal teeth in an aberrant specimen of the small Africanbarb Barbus paludinosus (Cyprinidae): novelty or atavisticalteration? J Fish Biol 67, 286–291.

Grammatopoulos GA, Bell E, Toole L, Lumsden A, Tucker AS (2000)Homeotic transformation of branchial arch identity after Hoxa2overexpression. Development 127, 5355–5365.

Graveson AC (1993) Neural crest: contributions to the develop-ment of the vertebrate head. Am Zool 33, 424–433.

Graveson AC, Smith MM, Hall BK (1997) Neural crest potential fortooth development in a urodele amphibian: developmental andevolutionary significance. Dev Biol 188, 34–42.

Hall BK (2000) The neural crest as a fourth germ layer and verte-brates as quadroblastic not triploblastic. Evol Dev 2, 3–5.

Hall BK (2005) Skeletal biology in an Evo-Devo-Paleo lab. PalaeontolNewsletter 59, 26–34.

Hall BK (2007) Homoplasy and homology: Dichotomy or continuum?J Human Evol 52, 473–479.

Hall BK, Witten PE (2007) The origin and plasticity of skeletaltissues in vertebrate evolution and development. In MajorTransitions in Vertebrate Evolution (eds Anderson JS, Sues H-D),pp. 13–56. Bloomington: Indiana University Press.

Holmbakken N, Fosse G (1973) Tooth replacement in Gadus callarius.Z Anat Entwickl-Gesch 143, 65–79.

Hook RW (1983) Colosteus scutellatus (Newberry), a primitivetemnospondyl amphibian from the Middle Pennsylvanian ofLinton, Ohio. Am Mus Novit 2770, 1–41.

Huysseune A (1995) Phenotypic plasticity in the lower pharyngealjaw dentition of Astatoreochromis alluaudi (Teleostei: Cichlidae).Arch Oral Biol 40, 1005–1014.

Huysseune A (2006) Formation of a successional dental lamina inthe zebrafish (Danio rerio): support for a local control ofreplacement tooth initiation. Int J Dev Biol 50, 637–643.

Huysseune A, Sire J-Y (1997) Structure and development of teethin three armoured catfish, Corydoras aeneus, C. arcuatus andHoplosternum littorale (Siluriformes, Callichthyidae). Acta Zool78, 69–84.

Huysseune A, Sire J-Y (1998) Evolution of patterns and processesin teeth and tooth-related tissues in non-mammalian verte-brates. Eur J Oral Sci 106 (Suppl. 1), 437–481.

Huysseune A, Witten PE (2008) An evolutionary view on toothdevelopment and replacement in wild Atlantic salmon (Salmosalar L.). Evol Dev 10, 6–14.

Huysseune A, Takle H, Soenens M, Taerwe K, Witten PE (2008)Unique and shared gene expression patterns in Atlantic salmon(Salmo salar) tooth development. Dev Genes Evol 218, 427–437.



475

Imai N, Osumi N, Eto K (1998) Contribution of foregut endodermto tooth initiation of mandibular incisor in rat embryos. Eur JOral Sci 106 (Suppl. 1), 19–23.

Jackman WR, Stock DW (2006) Transgenic analysis of Dlx regula-tion in fish tooth development reveals evolutionary retention ofenhancer function despite organ loss. Proc Natl Acad Sci USA103, 19390–19395.

Jackman WR, Draper BW, Stock DW (2004) Fgf signaling is requiredfor zebrafish tooth development. Dev Biol 274, 139–157.

James CT, Ohazama A, Tucker AS, Sharpe PT (2002) Toothdevelopment is independent of a Hox patterning programme.Dev Dyn 225, 332–335.

Janvier P (1996) Early Vertebrates. Oxford Monographs on Geologyand Geophysics 33. Oxford: Clarendon Press.

Janvier P (2007) Homologies and evolutionary transitions in earlyvertebrate history. In Major Transitions in Vertebrate Evolution(eds Anderson JS, Sues H-D), pp. 57–121. Bloomington: IndianaUniversity Press.

Jarvik E (1980) Basic Structure and Evolution of Vertebrates.Vol. 1. London: Academic Press.

Johanson Z, Smith MM (2003) Placoderm fishes, pharyngeal den-ticles, and the vertebrate dentition. J Morphol 257, 289–307.

Johanson Z, Smith MM (2005) Origin and evolution of gnathos-tome dentitions: a question of teeth and pharyngeal denticlesin placoderms. Biol Rev 80, 303–345.

Jollie M (1968) Some implications of the acceptance of a delamina-tion principle. In Current Problems of Lower Vertebrate Phylogeny(ed. Ørvig T), pp. 89–107. Stockholm: Almqvist & Wiksell.

Kakizawa Y, Meenakarn W (2003) Histogenesis and disappearanceof the teeth of the Mekong giant catfish, Pangasianodon gigas(Teleostei). J Oral Sci 45, 213–221.

Kemp A (2002a) Amino acid residues in conodont elements. JPaleontol 76, 518–528.

Kemp A (2002b) Hyaline tissue of thermally unaltered conodontelements and the enamel of vertebrates. Alcheringa 26, 23–36.

Kemp NE (1999) Chapter 2. Integumentary System and Teeth. InSharks, Skates, and Rays. The Biology of Elasmobranch Fish (ed.Hamlett WC), pp. 43–68. Baltimore: The Johns Hopkins UniversityPress.

Kimmel CB, Eberhart JK (2008) The midline, oral ectoderm, and thearch-0 problem. Integr Comp Biol 48, 668–680.

Kurtén B (1963) Return of a lost structure in the evolution of thefelid dentition. Soc Scient Fenn Comment Biol B 26, 1–12.

Laurenti P, Thaeron-Antono C, Allizard F, Huysseune A, Sire J-Y(2004) The cellular expression of eve1 suggests its requirementfor the differentiation of the ameloblasts, and for the initiationand morphogenesis of the first tooth in the zebrafish (Daniorerio). Dev Dyn 230, 727–733.

McCollum M, Sharpe PT (2001) Evolution and development ofteeth. J Anat 199, 153–159.

Meyer A (1999) Homology and homoplasy: the retention ofgenetic programmes. In Homology (eds Bock GR, Cardew G),pp. 141–157. Chichester: John Wiley & Sons.

Miles AEW, ed. (1967) Structural and Chemical Organization ofTeeth. New York: Academic Press.

Miller RF, Cloutier R, Turner S (2003) The oldest articulatedchondrichthyan from the early Devonian period. Nature 425,501–504.

Millot J, Anthony J (1958) Anatomie de Latimeria chalumnae.Tome I. Squelette, muscles et formation de soutien. Paris: CNRS.

Morris SC (1980) Conodont function: fallacies of the tooth model.Lethaia 13, 107–108.

Nelson GJ (1969) Gill arches and the phylogeny of fishes, withnotes on the classification of vertebrates. Bull Am Mus Nat Hist141, 475–552.

Nelson GJ (1970) Pharyngeal denticles (placoid scales) of sharks,with notes on the dermal skeleton of vertebrates. Am Mus Novit2413, 1–26.

Ørvig T (1967) Phylogeny of tooth tissues. Evolution of some calcifiedtissues in early vertebrates. In Structural and Chemical Organi-zation of Teeth (ed. Miles AEW), Vol. 1, pp. 45–110. London:Academic Press.

Owen R (1840–1845) Odontography. London: Hippolyte Balliere.Peyer B (1968) Comparative Odontology. Chicago: University

Press.Pietsch TW, Orr JW (2007) Phylogenetic relationships of deep-sea

anglerfishes of the suborder Ceratioidei (Teleostei: Lophiiformes)based on morphology. Copeia 2007, 1–34.

Piotrowski T, Nüsslein-Volhard C (2000) The endoderm plays animportant role in patterning the segmented pharyngeal regionin zebrafish (Danio rerio). Dev Biol 225, 339–356.

Pridmore PA, Barwick RE, Nicoll RS (1996) Soft anatomy and theaffinities of conodonts. Lethaia 29, 317–328.

Prince VE, Joly L, Ekker M, Ho RK (1998) Zebrafish hoxgenes:genomic organization and modified colinear expression patternsin the trunk. Development 125, 407–420.

Purnell MA (2001) Feeding in extinct jawless heterostracan fishesand testing scenarios of early vertebrate evolution. Proc R SocLond B 269, 83–88.

Raikow RJ, Borecky SR, Berman SL (1979) The evolutionary re-establishment of a lost ancestral muscle in the bowerbirdassemblage. Condor 81, 203–206.

Reif WE (1982) Evolution of dermal skeleton and dentition invertebrates. The odontode regulation theory. Evol Biol 15, 287–368.

Reif WE (2002) Evolution of the dermal skeleton of vertebrates:Concepts and methods. Neues Jahrb Geol Paläont Abh 223, 53–78.

Reif WE (2006) Conodonts, odontodes, stem-groups, and theancestry of enamel genes. Neues Jahrb Geol Paläont Abh 241,405–439.

Rijli FM, Mark M, Lakkaraju S, Dierich A, Dollé P, Chambon P (1993)A homeotic transformation is generated in the rostral branchialregion of the head by disruption of Hoxa-2, which acts as a selectorgene. Cell 75, 1333–1349.

Schilling TF, Piotrowski T, Grandl H, et al. (1996) Jaw and branchialarch mutants in zebrafish. I. Branchial arches. Development 123,329–344.

Schoch RR (2001) Can metamorphosis be recognised in Palaeozoicamphibians? Neues Jahrb Geol Paläont Abh 220, 335–367.

Schoch RR (2002) The evolution of metamorphosis in temnospondyls.Lethaia 35, 309–327.

Scott HW (1934) The zoological relationships of the conodonts. JPaleontol 8, 448–455.

Sellman S (1946) Some experiments on the determination of thelarval teeth in Ambystoma mexicanum. Odontol Tidskr 54, 1–128.

Sire J-Y (2001) Teeth outside the mouth in teleost fishes: how tobenefit from a developmental accident. Evol Dev 3, 104–108.

Sire J-Y, Allizard F (2001) A fourth Teleost lineage possessingextra-oral teeth: The genus Atherion (Teleostei; Atherini-formes). Eur J Morphol 39, 295–305.

Sire J-Y, Davit-Béal T, Delgado S, Van der heyden C, Huysseune A(2002) First-generation teeth in nonmammalian lineages: Evi-dence for a conserved ancestral character? Microsc Res Techn59, 408–434.



476

Sire J-Y, Donoghue PCJ, Vickaryous MK (2009) Origin and evolutionof the integumentary skeleton in non-tetrapod vertebrates.J Anat 214, 409–440.

Sire J-Y, Huysseune A (1996) Structure and development of theodontodes in an armoured catfish, Corydoras aeneus (Siluriformes,Callichthyidae). Acta Zool 77, 51–72.

Sire J-Y, Marin S, Allizard F (1998) Comparison of teeth and dermaldenticles (odontodes) in the teleost Denticeps clupeoides(Clupeomorpha). J Morphol 237, 237–255.

Smith MM (2003) Vertebrate dentitions at the origin of jaws:when and how pattern evolved. Evol Dev 5, 394–413.

Smith MM, Coates MI (1998) Evolutionary origins of the vertebratedentition: phylogenetic patterns and developmental evolution.Eur J Oral Sci 106 (Suppl. 1), 482–500.

Smith MM, Coates MI (2000) Evolutionary origins of teeth andjaws: Developmental models and phylogenetic patterns. InDevelopment, Function and Evolution of Teeth (eds Teaford M,Smith M, Ferguson M), pp. 133–151. Cambridge: CambridgeUniversity Press.

Smith MM, Coates MI (2001) The evolution of vertebrate dentitions:phylogenetic pattern and developmental models. In MajorEvents in Early Vertebrate Evolution (ed. Ahlberg PE), SystematicsAssociation Special Volume Series 61, 223–240.

Smith MM, Hall BK (1990) Development and evolutionary originsof vertebrate skeletogenic and odontogenic tissues. Biol Rev 65,277–373.

Smith MM, Johanson Z (2003a) Separate evolutionary origins ofteeth from evidence in fossil jawed vertebrates. Science 299,1235–1236.

Smith MM, Johanson Z (2003b) Response to comment on ‘Separateevolutionary origins of teeth from evidence in fossil jawedvertebrates’. Science 300, 1661c.

Soukup V, Epperlein HH, Horacek I, Cerny R (2008) Dual epithelialorigin of vertebrate oral teeth. Nature 455, 795–799.

Stiassny MLJ (1991) Atavisms, phylogenetic character reversals,and the origin of evolutionary novelties. Neth J Zool 42, 260–276.

Stock DW (2001) The genetic basis of modularity in the develop-ment and evolution of the vertebrate dentition. Philos Trans RSoc Lond B 356, 1633–1653.

Stock DW (2007) Zebrafish dentition in comparative context. J ExpZool 308B, 523–549.

Stock DW, Jackman WR, Trapani J (2006) Developmental geneticmechanisms of evolutionary tooth loss in cypriniform fishes.Development 133, 3127–3137.

Ströer WFH (1933) Experimentelle Untersuchungen über dieMundentwicklung bei den Urodelen. W Roux’ Arch Entw Mech130, 131–186.

Teaford M, Smith M, Ferguson M, eds (2000) Development, Functionand Evolution of Teeth. Cambridge: Cambridge University Press.

Thenius E (1989) Zähne und Gebiss der Säugetiere. In Handbuchder Zoologie (eds Niethammer J, Schliemann H, Starck D),pp. 1–513. Berlin: Walter de Gruyter.

Trotter JA, FitzGerald JD, Kokkonen H, Barnes CR (2007) Newinsights into the ultrastructure, permeability, and integrity ofconodont apatite determined by transmission electron micros-copy. Lethaia 40, 97–110.

Van der Brugghen W, Janvier P (1993) Denticles in thelodonts.Nature 364, 107.

Van der heyden C, Huysseune A (2000) Dynamics of tooth forma-tion and replacement in the zebrafish (Danio rerio) (Teleostei,Cyprinidae). Dev Dyn 219, 486–496.

Vandewalle P, Huysseune A, Aerts P, Verraes W (1994) Thepharyngeal apparatus in teleost feeding. In Biomechanics ofFeeding in Vertebrates (eds Bels V, Chardon M, Vandewalle P),Adv Comp Env Physiol 18, 59–92.

Warga RM, Nüsslein-Volhard C (1999) Origin and development ofthe zebrafish endoderm. Development 126, 827–838.

Wilde CE (1955) The urodele neuroepithelium. I. The differentiationin vitro of the cranial neural crest. J Exp Zool 130, 573–591.

Wise SB, Stock DW (2006) Conservation and divergence of Bmp2a,Bmp2b, and Bmp4 expression patterns within and betweendentitions of teleost fishes. Evol Dev 8, 511–523.

Witten PE, Hall BK, Huysseune A (2005) Are breeding teeth inAtlantic salmon a component of the drastic alterations of theoral facial skeleton? Arch Oral Biol 50, 213–217.

Yelick PC, Schilling TF (2002) Molecular dissection of craniofacialdevelopment using zebrafish. Crit Rev Oral Biol Med 13, 308–322.

Young GC (2003) Did placoderm fish have teeth? J Vert Paleontol23, 987–990.

Zhuravlev AV (2005) Specific features of the hard tissues of latepaleozoic conodont elements. Paleontol J 39, 289–293.

review evolutionary and developmental origins of the ...jysire.free.fr/pdf/pdf...

Documents