Stability versus diversity of the dentition during evolutionary radiation in cyprinine fish

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Evolutionary radiations, especially adaptive radiations, have been widely studied but mainly for recent events such as in cichlid fish or Anolis lizards. Here, we investigate the radiation of the subfamily Cyprininae, which includes more than 1300
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  rspb.royalsocietypublishing.org Research Cite this article:  Pasco-Viel E, Yang L, VeranM, Balter V, Mayden RL, Laudet V, Viriot L.2014 Stability versus diversity of the dentitionduring evolutionary radiation in cyprinine fish. Proc. R. Soc. B  281 : 20132688.http://dx.doi.org/10.1098/rspb.2013.2688Received: 15 October 2013Accepted: 16 January 2014 Subject Areas: evolution, ecology Keywords: Cypriniformes, X-ray microtomography,ecological speciation, dental morphology Author for correspondence: Laurent Viriote-mail: laurent.viriot@ens-lyon.fr † Present address: Hollings Marine Laboratory,Charleston, SC 29412, USA.Electronic supplementary material is availableat http://dx.doi.org/10.1098/rspb.2013.2688 orvia http://rspb.royalsocietypublishing.org. Stability versus diversity of the dentitionduring evolutionary radiation incyprinine fish Emmanuel Pasco-Viel 1 , Lei Yang 3,† , Monette Veran 4 , Vincent Balter 5 ,Richard L. Mayden 3 , Vincent Laudet 2 and Laurent Viriot 1 1 Evo-devo of Vertebrate Dentition, and  2 Molecular Zoology, Institut de Ge´nomique Fonctionnelle de Lyon (IGFL),UMR CNRS 5242, Universite´ de Lyon, Universite´ Claude Bernard Lyon 1, Ecole Normale Supe´rieure de Lyon, Lyon,France 3 Department of Biology, Saint Louis University, St Louis, MO 63103, USA 4 Centre de Recherches sur la Pale´obiodiversite´ et les Pale´oenvironnements (CRP2), De´partement Histoire de laTerre, UMR CNRS 7207, Muse´um National d’Histoire Naturelle, Paris, France 5 Laboratoire de Ge´ologie de Lyon (LGLTPE), UMR CNRS 5276, Universite´ de Lyon, Universite´ Claude BernardLyon 1, Ecole Normale Supe´rieure de Lyon, Lyon, France Evolutionary radiations, especially adaptive radiations, have been widelystudied but mainly for recent events such as in cichlid fish or  Anolis  lizards.Here, we investigate the radiation of the subfamily Cyprininae, whichincludes more than 1300 species and is estimated to have srcinated fromSoutheast Asia around 55 Ma. In order to decipher a potential adaptive radi-ation, within a solid phylogenetic framework, we investigated the trophicapparatus, and especially the pharyngeal dentition, as teeth have provedto be important markers of ecological specialization. We compared twotribes within Cyprininae, Poropuntiini and Labeonini, displaying divergentdental patterns, as well as other characters related to their trophic apparatus.Our results suggest that the anatomy of the trophic apparatus and diet areclearly correlated and this explains the difference in dental patterns observed between these two tribes. Our results illustrate the diversity of mechanismsthat account for species diversity in this very diverse clade: diversification of dental characters from an ancestral pattern on the one hand, conservationof a basal synapomorphy leading to ecological specialization on the otherhand. By integrating morphological, ecological and phylogenetic analyses,it becomes possible to investigate ancient radiation events that haveshaped the present diversity of species. 1. Introduction One crucial question in evolution deals with patterns and processes underlyingevolutionary radiations involving rapid bursts of speciation [1–3]. Multiple cases of radiation events have been linked to the rapid diversification of adap-tive phenotypes [4,5]. Notable examples of recent adaptive radiations are provided by cichlid fish in Eastern African lakes [6],  Anolis  lizards in the Carib- bean Islands [7] and Darwin finches in the Galapagos Islands [8]. These classical cases illustrate how radiations can be related to habitat and diet diver-sification, and/or to cases of sexual selection, driving rapid speciation [9].However, evolutionary radiations have not been confined to recent events.Careful examination of phylogenetic trees reveal more ancient radiationevents for which factors contributing to species diversification remain more elu-sive [10,11]. Thus, investigations of more ancient radiations will help to understand cases of rapid diversification of clades recognized as supragenerictaxonomic ranks.In order to investigate the potential role played by ecological speciationduring radiations, whether an evolutionary radiation is adaptive or non-adaptive, it is crucial to focus on characters that provide proxies for assessing biological niches occupied by species. The question is whether or not the & 2014 The Author(s) Published by the Royal Society. All rights reserved.  diversification of species is correlated to the adaptation todifferent environments. In this framework, dentition con-stitutes a major character for assessing adaptive radiation asits shape and arrangement play a key role in food captureand processing. The diversification of the dentition withina diversified clade strongly suggests that this clade hasundergone divergent natural selection, leading to ecologicalspeciation. Particularly in mammals, it has been shown thatdentition pattern, individual tooth shape and dental inter-locking are closely related to various food habits, and toothcrown shape is frequently used as a marker of ecologicaladaptation [12–14]. Dentition diversification can therefore reliably reflect changes in the life history of species, thusmaking this character a good indicator for developing andtesting hypotheses as to changes in ecological preferenceswithin the evolution of a clade [15].Here, we aim to examine the factors that could explain theecomorphological diversification of the Cyprininae fromthe Mekong Basin, one of the World’s most diverse riverineecosystems. Within the order Cypriniformes, which encom-passes about 4000 species [16,17], the subfamily Cyprininae includes about 1300 species [18] mainly distributed in Southand East Asia, a region hypothesized as the cradle for theorder [19]. All Cypriniformes are characterized by the absenceof oral teeth and the presence of two symmetrical sets of phar-yngeal teeth located on the right and left parts of the fifthceratobranchial arch [20]. Right and left sets of pharyngealteeth do not interlock but together occlude against a kerati-nized chewing pad (KCP) that covers the pharyngeal plate of the basioccipital [21]. Across the order, there is great diversityin the arrangement, number and shape of pharyngeal teeth[22]. Some species have one row encompassing numerousteeth while others have three rows with fewer teeth on eachrow. In addition, the pharyngeal tooth crown varies from asimple cone to a complex multicuspid pattern [22].To carry out this study, it was essential to build a solidphylogeneticframeworkforthesubfamilyCyprininae,encom-passing several well-supported monophyletic groups. Amongthese lineages, we studied two monophyletic tribes that areparticularly diverse: Labeonini (400 species) and Poropuntiini(100 species) [18,23]. The Poropuntiini include species mainly restricted to Southeast Asia (Burma, Thailand, Laos,Cambodia, Vietnam, Malaysia and Indonesia), whereas theLabeonini includes species living from East Asia to Africa[24]. We chose to investigate these two tribes because of theinfluence of geographical extension in species diversificationand their ecological diversity in a same geographical region.Our first goal wasto evaluatewhether the difference in speciesnumber between Labeonini and Poropuntiini is a consequenceof the difference in geographic distribution between the twotribes. Our second goal was to test whether the radiation in acommon geographical area (here, Southeast Asia) is adaptiveor not, through adaptation to various food habits, which can be recorded by scrutinizing changes in dental morphology. 2. Results (a) Phylogeny of the Cyprininae We built a phylogeny of 103 species of Cyprinidae usingfive mitochondrial genes (electronic supplementary material,table S1 and figure S2). Nuclear markers were not included inthisphylogeneticanalysisaspolyploidyoccursinseveralcypri-nine lineages, thus rendering nuclear markers unreliable [25].Cyprinidae are divided into nine subfamilies, among whichCyprininae is the most diverse with more than 1300 species[18].WithintheCyprininae,weidentifiedsevenwell-supportedmonophyletic tribes, including Poropuntiini and Labeonini(electronic supplementary material, figure S2). As there are nopolyploid species in Poropuntiini and Labeonini, two mito-chondrial (Cytb, COI) and two nuclear (Rag1, Rho) markerswere used to build a more comprehensive tree for 17 speciesfrom 10 genera of Labeonini and 22 species from 16 genera of Poropuntiini (figure 1; electronic supplementary material,figure S3 and table S1). The tribe Poropuntiini splits up intothree robust and early diverging monophyletic subtribes that 1001001009689100100BarbonyminaCosmochilinaPoropuntiinaPoropuntiiniLabeoina LabeoniniSemilabeoinaGarrainaOsteochilinaoutgroupsMa32.840.655.210010099100100 Puntius -clade  Barbus -clade Figure 1.  Summarized phylogeny of Cyprininae focusing on Poropuntiini and Labeonini. Phylogeny of Cyprininae, including Poropuntiini and Labeonini, based onML and Bayesian analyses (electronic supplementary material, figure S2), using mitochondrial (Cytb, COI) and nuclear (Rag1, Rho) markers. Bootstrap values from MLanalyses are provided above nodes. Molecular dating of clades is also provided and is based on the electronic supplementary material, figure S3. Geographicalextension is shown for the two tribes. r     s      p   b      .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b     l       i        s   h     i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1     3    2     6     8     8     2  we named Cosmochilina, Poropuntiina and Barbonymina(figure 1). The tribe Labeonini divides up into four early diver-ging subtribes previously described as Garraina, Labeonina,Osteochilina and Semilabeoina [23].Moleculardatinganalyses forthephylogenyofCyprininaewere performed using mitochondrial data (see the electronicsupplementary material, text S10 and figure S4). They werecalibrated using four different fossil taxa:  Labeo  (17.0 Ma), Cyprinus  (33.9 Ma),  Puntius  (28.4–37.2 Ma) and the oldestcyprinid fossil ( Parabarbus , 48.6 Ma). Divergence time esti-mation, conducted using Bayesian analyses (see Material andmethods), clearly supported that the subfamily Cyprininaediverged at 55 Ma (95% CI: 47–66 Ma). The tribe Labeoninidiverged at 40 Ma (95% CI: 33–49 Ma), whereas the tribePoropuntiini diverged more recently at 33 Ma (95% CI: 26–40 Ma; see figure 1 and the electronic supplementary material,figure S4). (b) Comparative anatomy of the pharyngealfeeding apparatus The anatomyof the pharyngeal dental system was investigatedusing X-ray microtomography for each species of Poropuntiiniand Labeonini included in the electronic supplementarymaterial, figure S2 phylogenetic analysis. Microtomographyprovides high-resolution three-dimensional reconstructions of mineralized tissues [22,26], allowing the virtual segmentation and investigation of both pharyngeal bones and teeth, but notthe KCP. Thus, it was possible to scrutinize the number andarrangement of pharyngeal teeth, as well as individual shapeof tooth crowns. Two to four specimens were examined foreachspeciesinordertoavoidpotentialintraspecificpolymorph-isms although previous studies have shown that cyprinidintraspecific polymorphism in tooth number is low [27]. (i) Tooth number Pharyngeal teeth on both left and right pharyngeal bones areorganized in several rows, from one to three tooth rows inCyprininae [22,28]. Most species have three dental rows [22], named internal, medial and external rows. The internalrow, or main row, always comprises the highest number of teeth. In each row, the number of teeth is variable (seefigure 2). We recorded neither left versus right asymmetryin tooth number contrary to what is reported in other cypri-nid clades [22], nor intraspecific polymorphism. Thus, thedental formula can be established from one set of pharyngeal  IncisilabeobehriCyclocheilichthysarmatus 2,4,5-5,4,22,3,5-5,3,2LabeoniniPoropuntiini ScaphognathopsstejnegeriPuntioplites falcifer  postero-ventral viewdorsal view,dental formuladetailedview3,5-5,32,3,4-4,3,2 Figure 2.  Comparison of pharyngeal dentition between Labeonini and Poropuntiini. Pharyngeal bones bearing pharyngeal teeth are shown in three different views:postero-ventral, dorsal and detailed view of teeth. In the dorsal view, the dental formula is indicated, as well as the position of the first tooth on the main row(indicated by arrows), which can be small or absent in Poropuntiini (see text). Scale bar is 1 mm. r     s      p   b      .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b     l       i        s   h     i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1     3    2     6     8     8     3  teeth and considered as symmetrical. Both number of toothrows and number of teeth per row are consistent at the gen-eric level, but they may vary between various genera(see figure 2).All investigated Labeonini have the same number of tooth rows andthesamenumberofteeth perrow, recapitulatedin the dental formula [5,4,2] (figure 2). On the contrary, thedental formula was variable between Poropuntiini genera(figure 2). The most common dental formula is [5,3,2] butwe observed genera with only one or two tooth rows (see Scaphognathops  in figure 2) as well as genera with only fourteeth on the internal row (see  Puntioplites  in figure 2). Althoughhalf of studied genera display a [5,3,2] dental formula, theother half show substantial variations leading to the followingdental formula for Poropuntiini: [4-5,0-3,0-2]. Thus, there is astriking contrast between the stability of dental formula inLabeonini as opposed in intergeneric diversity of this characterin Poropuntiini. (ii) Tooth arrangement In Labeonini, tooth crowns of each pharyngeal bone are veryclose to one another (see Labeonini dentitions on the electronicsupplementary material, figure S5) so that they together formtwo compact pavements which act like grinders by occludingagainst the KCP [29]. The grinding function is demonstrated by the abraded crown tips and by the occurrence of exposeddentine on all flattened occluding surfaces, except those of neoformed replacement teeth (see figure 2 and the electronicsupplementary material, figure S5). Exceptions to this pat-tern can be seen in  Garra  and  Mekongina , in which toothcrowns are more spaced (see the electronic supplementarymaterial, figure S5). On the contrary, Poropuntiini displaywell-separated rows of pharyngeal teeth whose crowns areusually pointed and weakly abraded (figure 2 and the electro-nic supplementary material, figure S5). An exception to thispattern is  Amblyrhynchichthys  in which teeth are closer to oneanother and crown tips slightly abraded, similar to Labeonini(see the electronic supplementary material, figure S5). More-over, in Poropuntiini, the first dental position of the mainrow is always occupied by a tiny tooth, much smaller thanother teeth of the same row (see arrows in figure 2). Thistooth is even lacking in seven out of 16 poropuntiine genera,so that the internal row only counts four teeth. This suggeststhat the first internal tooth, which will never occlude againstthe chewing pad given its size, could be lost by relaxed con-straints applied on this position. On the contrary, the firsttooth of the internal row is always present in Labeonini, andit fully participates in the grinding pavement. (iii) Tooth crown shape Each pharyngeal dental set of Cyprinidae is composed of teeththat have neither exactly the same size nor the same shape. Inthis regard, all Cyprinidae are clearly heterodont. Shape andsize of teeth can feebly vary from one position to another asin  Poropuntius  (see the electronic supplementary material,figure S5), but this variation can also be slightly more substan-tial as in  Discherodontus  (electronic supplementary material,figure S5). In order to circumvent this problem of individualdental variation, we established the representative crown phe-notypeforeach species basedonlyon the shapeof the twofirstdistal replacement teeth of the internal row, as replacementteeth do not show any sign of wear (electronic supplementarymaterial, figure S5).We hypothesized in a previous work [22] that the likely basal condition of tooth crown in Cyprinidae is a hooked- bicrested spoon (HBS) pattern, in which the crown is basicallymadeofasingleconicalcurvedcuspthatbearsaninternalcon-cave surface laterally flanked by two crests running from thetip of the cusp to the bottom of the concave surface. Thisphenotype is well documented in  Cyclocheilichthys  (figure 2).Our morphological investigationsshowed that crown shapeis highly diversified in Poropuntiini. Their crown shape likelyradiated from the HBS pattern, which is the most commonphenotypeacrossthetribe(seefigure2andtheelectronicsupple-mentary material, figure S5).  Balantiocheilos ,  Cyclocheilichthys , Poropuntius  and  Hypsibarbus  have a crown phenotype veryclose to the typical HBS shape. ‘ Barbonymus ’  gonionotus  and Puntioplites  show a trend of the HBS pattern toward a strongreinforcement of the crests as well as of the curvature of thecrown tip, resulting in a ‘Phrygian hat’ pattern.  Barbonymusaltus ,  Cyclocheilos  and  Mystacoleucus  display a HBS patternwith the addition of a second lesser developed cusp, which islocated at the base of the concave surface . Scaphognathops shows a great enlargement of the concave surface to the detri-ment of both cusp tip and lateral crests. The crown phenotyperesults in a shovel pattern perfectly documented in this genus. Cosmochilus  and  Albulichthys  display shovel crowns with theaddition of cingular cusps at the basis of the concave surface,whereas  Discherodontus  and  Sabwa  display a shovel patternwith conservation of a tiny pointed cusp at the crown tip.Two genera,  Sikukia  and  Amblyrhynchichthys , display morederived tooth shapes that are difficult to interpret in terms of evolutionarytrends. Sikukia displaysteethwithmuchreinforcedcrests along with a central groove and very abraded crowns.  Amblyrhynchichthys  displays teeth that have kept a small tipcusp but the general shape and arrangement makes it conver-gent with the dentition in Labeonini. Most Labeonini displayflat tooth crowns. Neoformed replacement teeth show thatunworn crown morphologies derive from the HBS pattern,from which the concave surface substantially expanded trans-versally. Occlusal surfaces are rapidly worn out so that thewhole set constitutes a unique pavement parallel to the KCP(see figure 3). Exceptions to this general pattern are  Garra  and  Mekongina  that likely conserved the basal characteristics for thetribe, in which crowns are moderately expanded and lessabraded, so that they do not constitute a compact pavement.Finally, crown shape evolution of Labeonini shows a trend inthe reinforcement of the lateral crests, which results in the bilo-phid crown pattern of   Cirrhinus ,  Henicorhynchus ,  Labiobarbus and  Osteochilus.  To sum up, although crown shape of Poro-puntiini and Labeonini are likely to both derive from the HBSpattern,Poropuntiinidisplayaradiativediversityincludingmul-tiple cases of convergence while Labeonini mainly evolvedtowards one direction, which seems highly constrained by thepavement arrangement of the dentition. (iv) Morphology of the fifth ceratobranchials Pharyngeal teeth of all Cypriniformes are attached to theright and left fifth ceratobranchial bones (FCB). Each FCB iscomposed of a dorsal branch, stretching perpendicularly tothe mesio-distal axis, and a ventral branch, pointing towardmesial direction. Teeth are located at the angle of these two branches. As in most clades of Cyprinidae, Poropuntiini r     s      p   b      .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b     l       i        s   h     i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1     3    2     6     8     8     4  display falciform FCB, with a curved dorsal branch. However,in Labeonini, FCB display a different shape, the ventral anddorsal branches being rather straight and perpendicular (seefigure 2).Outline morphometric analyses of FCB (electronic sup-plementary material, figure S6) show that Poropuntiini sharea same morpho-space together with other species of Cyprini-nae, Cultrinae and Danioninae, whereas Labeonini occupy aseparated morpho-space. Labeonini are discriminated fromother clades by the first axis of variation, which represents66.9% of the total variation. This latteraxis opposesthe slenderand falciform FCB of Poropuntiini and other Cyprinidae to therobust and perpendicular FCB of Labeonini. Exceptionsto thisdiscrimination are the FCB of   Garra  and  Mekongina , whichplot among Poropuntiini. This would suggest that  Garra  and  Mekongina  likely conserved some basal characteristics. (v) Height of the pharyngeal cavity A significant difference was detected in the relative size of the pharyngeal cavity between Labeonini and Poropuntiini(figure 3 and the electronic supplementary material, figure S7).TheheightofthepharyngealcavityofLabeoniniislow,meaningthat tooth tips are close to the KCP. This would suggest thatLabeonini feed on small particles, for example planktonicelements.Onthecontrary,thepharyngealcavityofPoropuntiiniis high, allowing them to feed on larger prey items. These ana-tomical observations were confirmed by significant biometricaldata: thepch/(pch þ pdh) ratio calculated between pharyngealcavity height (pch) and pharyngeal dentition height (pdh) wasequal to 0.30 for Poropuntiini and to 0.17 for Labeonini ( n ¼ 20for Poropuntiini,  n ¼ 15 for Labeonini,  p -value , 0.001; seethe electronic supplementary material, figure S7).  Sikukia  is theexception for Poropuntiini by having a low cavity (ratio equalto the mean ratio for Labeonini), and  Garra  and  Mekongina have a higher pharyngeal cavity than other Labeonini (ratioequal to 0.25 for both genera). (c) Mouth position The mouth of Labeonini is located on the ventral part of thehead and opens inferiorly, whereas Poropuntiini have a term-inal mouth, located at the rostral end of the fish and openingtowards the mesial direction (see figure 3). The position of themouth is an important character, which is directly linked todietandtrophic positionwithin thefoodweb.A mouthlocatedventrallysuggeststhat Labeoniniare eitherdemersalorbenthic bottom-feeders, mainly taking nutrients from the substratum[30]. On the contrary, a terminal mouth indicates that Labeoniniposition of themouthheight of pharyngeal cavitydiet omnivorouszoophagousphytophagousdetritivorousmicrophagous dentalformulatooth shapeconserved dental pattern diversity of dental phenotypesPoropuntiini 5,3,24,3,25,34,345,4,2expanded HBSPhrygian hatHBS+basal cuspshovelshovel+basal cuspshovel+pointed crown tipother shapes bilophidno pavement Figure 3.  Model of evolution of pharyngeal dentition in correlation with the trophic apparatus and diet. Labeonini and Poropuntiini differ in their mouth position,as well as the height of the pharyngeal cavity. For the position of the mouth, Labeonini is illustrated with  Mekongina erythropsila , and Poropuntiini with  Poropuntiuscarinatus . The arrows indicate the position of the mouth opening. These observations are congruent with data available on the diet of these species: in Labeonini,eight species are recognized as microphagous and one species as omnivorous, whereas in Poropuntiini, most species are omnivorous or zoophagous. All these factorscan be correlated with the difference in dental patterns (both tooth number and tooth shape) between the two groups. All categories of tooth shapes are describedin the text and detailed in the electronic supplementary material, figure S5. r     s      p   b      .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b     l       i        s   h     i       n     g   . o  r       g   P    r    o   c    .R     . S      o   c    . B     2    8   1     :    2     0    1     3    2     6     8     8     5
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