Speciation in Malagasy lemurs: a review of the cryptic ... · sportive lemurs, received little attention in molecular systematics (Ravaoarimanana et al., 2003). However, in the last

BASE Biotechnol. Agron. Soc. Environ.201418(4),577-588 Focus on:

SpeciationinMalagasylemurs:areviewofthecrypticdiversityingenusLepilemurLeslieWilmet(1),ChristophSchwitzer(2),PierreDevillers(3),RoselineC.Beudels-Jamar(3),CédricVermeulen(1)(1)UniversitédeLiège-GemblouxAgro-BioTech.DépartementBIOSE(IngénieriedesBiosystèmes).AxeGestiondesRessourcesForestières.PassagedesDéportés,2.B-5030Gembloux(Belgique).E-mail:[email protected](2)BristolZoologicalSociety.C/oBristolzooGarden.Clifton.BristolBS83HA(UK).(3)RoyalBelgianInstituteofNaturalSciences.ConservationBiologyTeam.ODNature.RueVautier,29.B-1000Brussels(Belgium).

ReceivedonMarch11,2013;acceptedonNovember5,2014.

Introduction.Madagascarisoneofthehighestbiodiversityhotspotsontheplanet;however,itisalsooneofthemostheavilyimpactedcountriesintheworldintermsofforestdegradationandgeneralhabitatdestruction.Literature.GenusLepilemur,infamilyLepilemuridae,isagenusofsmall,nocturnal,exclusivelyarborealMalagasyfolivores.Allspeciesinthegenushavesmallrangesofdistribution.Fullyforest-dependent,theyhaveahighriskofextinction.VariousmodelsandtheoriesofspeciationmechanismshavebeendevelopedforthefaunaandfloraofMadagascar.Forinstance,inthenorthwesternpartoftheisland,someauthorsusedLepilemurspp.totesttwoexistingmodelsofdistribution:the“Martinmodel”and“Wilmémodel”.Conclusion.RegardingtheimpactofforestdestructionandhabitatdegradationinMadagascar,conservationstrategiesforLepilemurneedtobeputinplace.ThispapergivesanoverviewofthecurrentknowledgeofthegenusLepilemurandexaminesspeciationforMalagasylemurs.Theunderstandingofspeciesdistributionwithinbiodiversityhotspotsisimportanttoidentifytargetforconservation.Therefore,wesummarizeandcomparethreebiogeographymodelsrelatedtolemursdistributioninordertounderstandthereasonsbehindthehighdiversity(26speciesintotal)amongthegenusLepilemur.ParticularattentionisalsogiventotheconceptofspeciesregardingbiodiversityissuesandthetaxonomicexplosioningenusLepilemur.Keywords.Lemurs,biogeography,models,forestdegradation,biodiversity,taxonomy,Madagascar.

Spéciation des lémuriens de Madagascar : synthèse sur l’énigmatique diversité du genre Lepilemur.Introduction.Madagascarestconsidérécommel’undesplusimportantshotspotsdebiodiversité,maiségalementcommel’undespayslesplustouchésentermesdedégradationdeshabitatsetdesforêts.Littérature.LafaunemammaliennedeMadagascarsecomposemajoritairementdeprimates,àsavoirleslémuriens.Parmieux,lafamilledesLepilemuridae,représentéeparungenreunique,Lepilemur,estungrouped’espècesnocturnes,exclusivementarboricolesetprincipalement folivores. Ilsontde trèspetitesairesdedistributionetsont fortementmenacésd’extinction.DifférentsmodèlesdemécanismesdespéciationontétédéveloppésàMadagascar,etdesauteursontanalyséladistributiondeLepilemurspp.surbasededeuxmodèlesbiogéographiquesexistants(«Martin model»et«Wilmé model»).LaquestiondelabiogéographiedeslepilemursaétéparticulièrementétudiéedansleNord-Ouestdel’ile.Conclusion.Suiteàl’impactdeladestructiondesforêtsetdeshabitatsàMadagascar,desstratégiesdeconservationdoiventêtremisesenplace.Cette revuedonneunaperçude l’étatactueldesconnaissancessur legenreLepilemuretanalyse lesprocessusimpliquésdanslaspéciationdeslémuriensdeMadagascar.Lacompréhensiondelarépartitiondesespècesdansleshotspotsdebiodiversitéestunfacteurclefpourl’établissementdesobjectifsdeconservation.Nousrésumonsetcomparonstroismodèlesbiogéographiques liés à ladistributiondes lémuriens afinde tenterde comprendre les raisonsde lagrandediversité(26autotal)dugenreLepilemur.Nousnousintéressonsauxconceptsd’espècedansuncontextedeconservation,ainsiqu’àlarécenteexplosiontaxonomiquepourlegenreLepilemur.Mots-clés.Lémur,biogéographie,modèle,dégradationdesforêts,biodiversité,taxonomie,Madagascar.

578 Biotechnol. Agron. Soc. Environ. 201418(4),577-588 WilmetL.,SchwitzerCh.,DevillersP.etal.

1. INTRODUCTION

Most of the plant and animal species found inMadagascar have evolved in long isolation and arefound nowhere else. Indeed, the island has beenseparatedfromAfricaforsome160millionyearsandfrom the Indian subcontinent for about 90millionyears (Ganzhorn et al., 2006; Vences et al., 2009).ThislongisolationpartlyexplainswhyMadagascarisoneofthehighestbiodiversityhotspotsontheplanet(Myersetal.,2000; Irwinetal.,2010).The tropicalandsubtropicalclimateof the island, its topographyanditsgeologicalhistory,togetherwithitsisolation,haveproducedauniquelevelofbothspeciesdiversityand endemism (Wilmé et al., 2006a; Irwin et al.,2010;Rogersetal.,2010).Morethan90%ofplants,92%ofreptiles,44%ofbirds,74%ofbutterflies,and100%ofamphibiansand terrestrialmammalsnativeto Madagascar are endemic (Vences et al., 2009).Unfortunately,Madagascarisalsooneoftheworld’smostheavilyimpactedareasintermsofrecenthabitatdestruction (Ganzhorn et al., 2006; Harper et al.,2007; Craul et al., 2009; Mittermeier et al., 2010;Mittermeier,2013).

Habitat fragmentation started with humanoccupationsome2,000yearsago(Crauletal.,2009)but ecosystemdestruction anddevastation increasedenormouslyduringthelastdecadesduetoahighrateofhumanpopulationgrowthandtofrequentpoliticalinstability (Mittermeieret al.,2010).Nearly90%ofthenaturalvegetationinMadagascarhasalreadybeenlost, and erosion on the island is severe (Ganzhornet al., 2000; Harper et al., 2007). Deforestation onMadagascar is massive, with around 100,000haper year lost (Méndez-Cárdenas et al., 2008),and remaining forests have become increasinglyvulnerable. Eighty percent of Madagascar’s forestsare now located within 1km of a non-forest edge(Schwitzer et al., 2013a).The dry deciduous forestsof western Madagascar are particularly affected(Ganzhornetal.,2000).Theislandisnowconsideredone of the most critical global priorities for natureconservation (Myers et al., 2000; Goodman et al.,2005). Obviously, the continuous decline of suchforest ecosystem is having a serious impact on allforest-dwelling organisms (Méndez-Cárdenas et al.,2008).Habitatlossandfragmentationareclearlyoneof the main causes of biodiversity loss worldwide(Fahrig,2003).

In recent years, numerous new plant and animalspecies have been revealed through surveys andanalyses on Madagascar. However, the fragilestatusofbothpreviouslyknownandnewlydetectedspecies has also been increasingly documented.Themammalian faunaofMadagascarmainlyconsistsoflemurian primates (Lemuroidea) (Randrianambinina

etal.,2010).Intheearly1980s,36speciesoflemurwere recognised on Madagascar (Tattersall, 1982),whereas today 98species (102taxa) are recognised(Mittermeier,2013).AnadditionalthreespecieshavebeendescribedsincethepublicationoftheHandbook,bringingthetotalofknownspeciesto101,comprising105taxa (Schwitzer et al., 2013b). A conservationstatusassessmentconductedinJuly2012foralllemursby thePrimateSpecialistGroup placed an alarming94outofthe103taxaknownatthetimeintooneofthe threatened categories of the International Unionfor Conservation of Nature (IUCN) classification.This is the highest ratio of threatened species everrecordedforalargegroupofmammals(Mittermeier,2013; Schwitzer et al., 2013a). The understandingof the diversity of genus Lepilemur, in familyLepilemuridae, has followed the trend observed forLemuroideaingeneral.Inthelastfewyears,alargenumberofnamedsubspeciesweregivenfullspeciesstatus(Vencesetal.,2009).Upto2006,only8speciesofLepilemurwereknown;26specieshavenowbeenidentifiedusingcytogeneticand/ormolecularmethods(Andriaholinirina et al., 2006; Louis et al., 2006;Rabarivolaetal.,2006;Mittermeieretal.,2010).

Evolutionarymechanismswerethesubjectofmanystudiestoexplainthehighspeciesrichnessintropicalfaunas.Avarietyofspeciationmodes(e.g.allopatricorsympatric,gradualor instantaneous,non-adaptiveordrivenbysexualselectionoradaptation)areknownto generate biotic diversity.Yet, themain drivers ofthe diversification process often remain unknown(Vences et al., 2009). Biogeographical approachesaddressfundamentalquestionsofglobalbiodiversitypatterns (Wiens et al., 2004). Graham et al. (2005)showedtheimportanceofhistoricalprocesses in theunderstanding of local biological diversity patterns,particularlyinthestudyofendemiclow-dispersaltaxa.Madagascariswellknowntobeagoodmodelregionfor the study of species diversification mechanisms(Vences et al., 2009). Indeed, many characteristicsof the country make it particularly suitable to testspecies diversification mechanisms proposed formany tropical regions (Yoder et al., 2006; Vencesetal.,2009).Vencesetal.(2009)describefivemaindiversification mechanisms for Madagascar: eco-geographic constraint, western rainforest refuges,riverine barrier, mountain refuges and watersheds.Severalbiogeographicalmodelshavebeendevelopedto address this question of high biodiversity of theisland.Manystudiesfocusedoncorrelationsbetweenlemur speciation and the biogeographical history ofMadagascar(Goodmanetal.,2004;Ganzhornetal.,2006;Wilmé et al., 2006;Yoder et al., 2006; Crauletal.,2007;Olivierietal.,2007).

The present paper aims to review speciationresearch inMadagascar, correlated to diversification

SpeciesdiversityandspeciationinLepilemur 579

mechanisms for Malagasy lemurs, to answerthe question “Why are there so many species ofLepilemur?”. First, we present an overview of thecurrentknowledgeofgenusLepilemur.Wesummarizethree biogeographic models related to MadagascarandLepilemurdiversity.The influenceof thechoiceof species concept on biodiversity evaluation isconsidered, in particular in relation to the so-calledtaxonomic inflation in genus Lepilemur and thecontroversiesithasgenerated.Toconductourreviewwe used databases such as Science Direct, JSTOR,SpringerLink,WileyandBioMedCentral.Westartedtheresearchwithtermssuchaslemurs,biogeographyandcrypticspecies,withoutanylimitontheyearofpublication.Theoldestpaperwefoundwaspublishedin 1972 and the more recent one was published in2013.

2. SPECIES DIVERSIFICATION IN MADAGASCAR: A CASE STUDY OF GENUS LEPILEMUR

2.1. Genus Lepilemur: what do we know?

Taxonomy. Genus Lepilemur I.Geoffroy, 1851, istheonlyextantgenusinfamilyLepilemuridaeGray,1870,oneoffivefamilies(Cheirogaleidae,Lemuridae,Lepilemuridae, Indriidae, Daubentoniidae) thatconstitute the infraorder Lemuriformes (suborderStrepsirrhini, order Primates), amonophyletic cladeendemic to Madagascar (Groves, 2001; Groves,2005; Horvath et al., 2007; Mittermeier, 2013;Schwitzer,2013b).Thisgenus,commonlyknownassportivelemurs,receivedlittleattentioninmolecularsystematics(Ravaoarimananaetal.,2003).However,in the last few years, several studies on lepilemurswereconductedinthewildandcorrelatedwithgeneticanalysis based on chromosomal rearrangements andmtDNA sequences (cf. section 3.2. of this paper).Thesestudiesresultedintheidentificationofanumberofnewspecies,andinducedsignificantchangesinthetaxonomyofthegenus(Ravaoarimananaetal.,2003;Andriaholinirinaetal.,2006;Rabarivolaetal.,2006;Crauletal.,2007;Mittermeieretal.,2010).

Morphology-diet.Sportivelemursaremedium-sizednocturnal,folivoreandexclusivelyarborealanimals.These vertical leapers and clingers generally weighless than 1kgwith, on average, a head-body lengthof20cmandataillengthof25cm(Leietal.,2008;Mittermeier et al., 2010;Mittermeier, 2013). In thewild,theidentificationoflepilemursspeciesislimitedby the lack of obvious phenotypic differentiationamong species (Ravaoarimanana et al., 2003;Andriaholinirinaetal.,2006).

Distribution, home range and density.Lepilemursare endemic to Madagascar. The 26currentlyidentifiedspeciesarewidelyanddiscreetlydistributedin thecountry’s low-andmid-altitudeevergreenanddeciduous forests (Andriaholinirina et al., 2006;Mittermeier et al., 2010). Each species appears tohaveaverysmallrange.Studiesonsomespeciesarestill tooscarcecompared to thosepertaining toothergeneraof lemurs, such as genusLemur (Mittermeieret al.,2010;Mittermeier,2013).Exactboundariesoftherangesofsomespeciesremainunknown,andneedfurther investigation (Louis et al., 2006;Craul et al.,2007;Mittermeier et al., 2010).There isnoestimateofpopulationsizeforanyspecies.Thesmallestforestfragmentoccupiedbyasportivelemur(i.e.Lepilemur ruficaudatus) seems to be around 6ha (Ganzhormetal.,2000;Seiler,2012).Becausesportivelemurshavethe lowest metabolic rate known among mammals,theirchoiceofsleepingsitesisparticularlyimportant(Schmidetal.,1996;Warrenetal.,1998;Seiler,2012).Activeduringthenight,theyspendthedayhiddenintreeholes,tanglesofbranchesandvines,or,asalastresort, in tree forks (Craul et al., 2009;Mittermeieretal.,2010;Seiler,2012).

Social structure and behaviour.Lepilemursareknownto be solitary, except two species (L. ruficaudatusandL. edwardsi) that live in pairs (Thalmann, 2001;Zinneretal.,2003).However,socialbehavior isstillunclearandmoredifferencesmayexistamongspecies(Mittermeier et al., 2010). Reproductive activity ofindividualspeciesisstillpoorlyknownbutL. edwardsishows a seasonal reproduction. This reproductivebehavior may be shared by other Lepilemur, withsome divergence linked to the latitudinal location ofthespeciesrange.Thereproductiverateislow,withamaximumofoneoffspringperyear.Sexualmaturityis reached after two years (Randrianambinina et al.,2007).

Threats. The main natural predators of lepilemursare the fossa (Chryptoprocta ferox), theMadagascarharrier-hawk (Polyboroides radius) and snakes(Acrantophis madagascariensis,Acrantophis dumeriliand Sanzinia madagascariensis) (Colquhoun, 2006).However,themainthreatcomesfromhumanactivities,particularly hunting and forest disturbance. Becausesportive lemurs are exclusively arboreal with verylimiteddistributions,theyareparticularlyaffectedbydeforestationandhabitatfragmentation,bothofwhichhave intensified in the last50years (Ganzhornetal.,2000;Harperetal.,2007;Schneideretal.,2010).Thesmallertheforestfragment,andthemoredisconnecteditbecomes,thegreatertheriskthatlemurpopulationsbecometoosmallandgoextinct(Fahrig,2003;Olivieriet al., 2005; Seiler, 2012). Habitat degradation also


means increasing visibility ofLepilemur in the wildand easier access for natural predators and hunters(Olivieri et al., 2005; Seiler, 2012). Forest qualitydetermines food quality and shelter availability forsportive lemurs. Forest fragmentation has a directimpactonpopulationsize,homerangesizeandgeneticisolationofsub-populations(Randrianambininaetal.,2010).TheavailabilityandqualityofMalagasyforestsis critical for the long-term survival of lepilemurs(Ganzhorn et al., 2000; Craul et al., 2007;Méndez-Cárdenasetal.,2008;Crauletal.,2009;Mittermeieretal.,2010;Randrianambininaetal.,2010).

Due to all the above factors, sportive lemurs areparticularly vulnerable to extinction. Further studiesarerequired togather informationandknowledgeonthisgenusinordertoformulateeffectiveconservationprograms (Olivieri et al., 2005; Rabarivola et al.,2006; Craul et al., 2007; Olivieri et al., 2007;Randrianambininaetal.,2007;Seiler,2012).

2.2. Speciation and diversification mechanisms of lemurs in Madagascar

Tropicalregionsharboralargebiologicaldiversity,andhavelongbeenregardedasideallocationstoinvestigategeneral speciation patterns and processes (Venceset al., 2009). The singularities of Madagascar makethis islandparticularly suitable to test hypotheses onspeciesdiversificationmechanismsdevelopedinothertropicalregions,anopportunitythathasonlyrecentlybeenfullyexploited(Grahametal.,2005;Vencesetal.,2009).Madagascarhasbeenisolatedfromotherlandmassesforaverylongtime(Irwinetal.,2010;Rogersetal.,2010).Theislandcanbedividedintofourwell-markedbioclimaticandphytogeographicdomains:– thesouthwesternsubaridspinyforest,– thewesterndrydeciduousforest,– theeasternandmontanerainforests,– the central subhumid grassland (Goodman et al., 2004;Vencesetal.,2009).

Highly specific faunas and floras are associatedwiththesemajorbiomes,whichareseparatedbysharpboundaries (Vences et al., 2009).Pleistocene climatevicissitudesandtheireffectsonforestdistributionandstructureshapedMadagascar’sspeciesdistributionandevolutionaryhistoryonrecent timescales (Ganzhornetal.,2006;Wilméetal.,2006;Vencesetal.,2009).These factors and the speciation mechanisms thatthey have flavored have been at the center ofmanystudies aiming at explaining the high degree ofmicroendemismontheisland(Goodmanetal.,2004;Ganzhornetal.,2006;Vencesetal.,2009).Manyofthese studies focused on Malagasy primates to testvarious diversification mechanisms (Vences et al.,2009). In particular, the possible role of the present

configuration andpast evolutionof the hydrographicsystem,knowntohavebeenanimportantfactorinthedistributionofprimatesintheneotropics(Ayeresetal.,1992;Lehman,2002),hasbeeninvestigated(Goodmanetal.,2004;Vencesetal.,2009).Speciationandcurrentdistribution of Malagasy lemurs have been studiedwithin the framework of two possible diversificationmechanisms, both based on the influence of rivers:the“riverinebarriermechanism”andthe“watershedsmechanism”(Goodmanetal.,2004;Ganzhornetal.,2006;Wilméetal.,2006a;Wilméetal.,2006b;Crauletal.,2007;Vencesetal.,2009).The“riverinebarriermechanism” hypothesis emphasizes the physicaldivisionbyariverofthecontinuousrangeofaspecies,leading tovicariantdivergence (Venceset al.,2009).Widthanddepthoftheriverandaltitudeofitssourceare significant characteristics (Goodmanet al., 2004;Vences et al., 2009). Several studies have shownthat large Malagasy rivers act as semi-permanentgeographical barriers for lemurs (Goodman et al.,2004;Ganzhornetal.,2006;Yoderetal.,2006;Craulet al., 2007; Vences et al., 2009). The “watershedmechanism”hypothesisconsidersriverbasinsasbioticrefugesduringclimaticvariation(Wilméetal.,2006a;Wilméetal.,2006b).Periodsofdrierclimateleadtoacontractionofforestsalongrivers.Twoscenariosexist.The first is applicable towatershedswith sources athighelevation.Theupperreachesofthesewatershedsact as retreat zones, between which connections aremaintained or established. These connections maypermit the dispersal and range expansion to otherbasins of species previously restricted to the lowercourseofastream.Suchretreat-dispersionwatershedsare expected to induce low levels of endemism.Thesecondscenariooccursinwatershedswithheadwatersatlowelevation.Forestblocksarereducedtoindividualriverine forests isolated by arid zones. These aridzonesactasbarrierstogeneflowforforest-dependentspecies,leadingtovicariantdivergenceandhighlevelsof endemism (Goodman et al., 2004; Wilmé et al.,2006a;Vencesetal.,2009).

2.3. Diversity of Malagasy lemurs: biogeographical models

Three biogeographical models have been developedto address the question of the high diversity ofMalagasy lemurs.All threemodels are based on thehypothesis thatmicroendemismmaybeexplainedbydiversification mechanisms, involving the past andpresenthydrographicsystemsofMadagascar(Martin,1972;Pastorinietal.,2003;Wilméetal.,2006a;Wilméetal.,2006b;Crauletal.,2009).Thefirstmodel,the“Martinmodel”,considerslargeriversasgeographicalbarrierstogeneflow,resultinginallopatricspeciation.ThismodeldividedMadagascarineightbiogeographic


Figure 1. A.MapofMadagascar showing the eight (letters in circles)main areas of lemur distribution according to the“Martinmodel”—Carte de Madagascar montrant les huit principales zones de distribution (lettres entourées de cercles) de lémurs selon le « Martin model »;B.Centreofendemism(numbersinsquares)ofthenorthernandnorthwesternMadagascaridentifiedinthe“Wilmémodel”—Centre de l’endémisme (nombres dans des carrés) du nord et du nort-ouest de Madagascar identifié selon le « Wilmé model »;C.MapofnorthwesternMadagascarshowingtheeightInter-River-SystemofCraul’s“largerivermodel”—Carte du nord-ouest de Madagascar montrant les huit systèmes inter-rivières du modèle de Craul « larges rivières ».Sources:A:modifiedfromPastorinietal.,2003—modifié d’après Pastorini et al., 2003 ;B,C:Crauletal.,2007.


zones, all separated by large rivers (Figure 1A)(Martin, 1972; Pastorini et al., 2003). This modelwas further refined and used to explain speciationwithin some lemur genera, such as Eulemur andPropithecus (Pastorini et al., 2003). The secondmodel, the “Wilmé model”, takes into account theeffect of quaternary paleoclimatic shifts on patternsofdispersalandvicarianceatintra-islandlevel.Thismodel shows the importance of riverine habitats inwatersheds acting as buffers for the maintenanceof local conditions, and as potential corridors forretreat towards higher altitudinal zones.Thismodelrecognises 12centres of endemism on Madagascar(Wilmé et al., 2006a; Wilmé et al., 2006b). Thethirdmodel, the“largerivermodel”,wasdevelopedbyCraul et al. (2007) to test predictionsof the twoprevious models on the distribution of Malagasymammals. This model focuses on genus Lepilemurin northern and northwestern Madagascar. Indeed,the genus, widely distributed in almost all forestedregions of the island, is particularly interesting fortesting biogeographic models. This model definedeight “Inter-River-Systems” (IRS): biogeographicalzones,whichcorrespondtoareasbetweeneightlargerivers(Figure 1C).Ontheonehand,theseriversactasbarrierstogeneflowleadingtocrypticspeciation.On the other hand they provide, during periodsof aridity, retreat zones in which small isolatedpopulations may become genetically differentiated,later recolonizing surrounding areas (Craul et al.,2007). In northern and northwestern Madagascar,the three models are largely complementary andare founded on similar hypotheses. However, someof the predictions of the threemodels are different.The “Martin model” predicts four biogeographiczones, which correspond well to the three deepestphylogeneticsplitsinCraul’s“largerivermodel”,butit fails to represent fully the speciesdiversity in thearea. The “Wilmé model” identifies a single centreofendemismbetweentheBetsibokaandMaevaranorivers(Figure 1B),anareainwhichCrauletal.(2007)locate three species of Lepilemur, all separated byrivers(Figure 1C).Craul’s“largerivermodel”seemstobestreflectthecomplexityofLepilemurdiversityanddistributionintheareaconsidered.Thiseffectoflargeriversasbiogeographicboundaries innorthernandnorthwesternMadagascarhasbeenshowntoalsoapply to mouse lemurs, Microcebus spp. (Olivierietal.,2007).

Complementaryresearchisstillneededtoconfirmthe relevance ofCraul’s “large rivermodel” and ofthefindingsofOlivierietal.(2007)toothertaxaandareas(Louisetal.,2006;Olivierietal.,2007;Venceset al., 2009).Validation in the field of suchmodelsbecomes unfortunately increasingly difficult in thefaceoftheintensivedestructionofforestedhabitats.

3. RECENT SPLITTING OF SPECIES IN GENUS LEPILEMUR

3.1. The concept of species regarding biodiversity issues

Species are “the units of the livingworld” (Groves,2011) and the perception of “species” is intuitive,centraltoallpopularclassificationsoflivingorganisms.Yet, a large number of species concepts focusing ondifferent properties, sometimes viewed as mutuallyexclusive, have been proposed and are in use. Theyare reviewed by, among others, de Queiroz (1998,1999,2007),Mallet(2007),Tattersall(2007),Wilkins(2008),Groves(2011),Grovesetal. (2011),Markolfetal. (2011)andMarkolfetal. (2013).Forprimates,thespeciesconceptsmostfrequentlyinvokedinrecentyears are theBiological SpeciesConcept (BSC), theRecognition Species Concept (RSC), the GeneticSpecies Concept (GSC), the Phylogenetic SpeciesConcept (PSC) and the General Lineage Concept.TheBiologicalSpeciesConcept (BSC)emphasizesa“harmoniousgeneticpool”protectedfromothersuchpoolsbyreproductiveisolatingbarriers(Alströmetal.,2003).Thebiologicalspeciesisdefined,onthebasisof reproductive isolation observed or estimated, as a“groupofactuallyorpotentiallyinterbreedingnaturalpopulations, which are reproductively isolated fromother such groups” (Mayr, 1942;Mayr, 1963;Mayr,1969). The Recognition Species Concept (RSC) isclosely related to the Biological Species Conceptthrough their common emphasis on reproductiveisolation mechanisms. Under the RSC, species arerecognizedbythepossessionofauniquespecificmaterecognitionsystem(SMRS).Aspeciesisdefinedasapopulation, or a group of populations, the membersof which share a common mate recognition system(Paterson,1978;Paterson,1985).

Contrary to the Biological Species Concept andrelated concepts, the Phylogenetic Species Concept(PSC), like the Evolutionary Species Concepts(Simpson,1961;Wiley,1978;Wiley,1981),ofwhichitconstitutesoneofthevariants,placesacentralemphasisontheevolutionaryfateoftaxainthepastandinthepresent. The phylogenetic species is defined as anirreducible (basal) cluster of organisms, diagnosablydistinct from other such clusters, and within whichthere is a parental pattern of ancestry and descent(Cracraft,1983,1987,1989).Examplesofconsistentuseof thePhylogeneticSpeciesConcept inmammaltaxonomy and demonstration of its operationaladvantageoverotherconceptsareofferedbyGroves(2001, 2011, 2012), Groves et al. (2011), Gippolitiet al. (2012), Gippoliti et al. (2013) and Cotterillet al. (2014). The Genetic Species Concept (GSC)focuses on isolation and divergence of gene pools.


Thegeneticspeciesisdefinedas“agroupofgeneticallycompatible interbreeding natural populations that isgenetically isolated fromother such groups” (Bradleyetal.,2001;Bakeretal.,2006).ThisdefinitionisveryclosetothatofthePSC.Bothdefinitionsincludegeneticindependence;bothaddacriterionofdiagnosabilitytoestablish evolutionary independence or speciation inprogress.WherethePSCallowsdiagnosabilitythroughanycharacters,theGSCrestrictsittogeneticmarkers.Moreover,thePSConlyrequiresdiagnosability,withoutreference to quantification of divergence, while theGSC places much emphasis on genetic distances todistinguishspeciesfromsimilarly-definedinfra-specificunits. In this, theGSC is similar to theMonophyleticSpecies Concept (Donoghue, 1985; Alström, 2002;Alströmetal.,2003)whichresortstodivergencetimestorankleast-inclusivetaxaaseithermonotypicspeciesorsubspeciesofapolytypicspecies(Alströmetal.,2003).Groves (2012) argues that ranking processes based ongeneticdistancesarehighlysubjective.Thesameistrueoftheevaluatedtimeofdivergence(Alströmetal.,2003).

Anentirelynewapproach to the conceptualizationofthespeciesnotionisproposedbydeQueiroz(1998,1999, 2005a, 2005b, 2005c, 2007), with the GeneralLineageConceptofSpeciesorUnifiedSpeciesConcept.Henotes thatallcontemporaryspeciesconceptssharea fundamental understanding of species as segmentsof lineages at the population level of biologicalorganization,anddifferonlyinthesecondaryproperties,which are regarded as necessary for consideringlineagestobespecies.Hesuggests(deQueiroz,2005a)that “a unified species concept can be achieved byinterpreting the common fundamental idea of beinga separately evolving lineage segment as the onlynecessarypropertyofspeciesandviewing thevarioussecondarypropertieseitheraslinesofevidencerelevantto assessing lineage separation or as properties thatdefine different subcategories of the species category(e.g., reproductively isolated species, monophyleticspecies, diagnosable species)”. This general lineageconcept is not an alternative to the various speciesconcepts,butamoregeneralconceptthatsubsumesallof them.The clarification of deQueiroz (1998) shiftsthephilosophicalcontroversiesoverspeciesconceptstomethodologicaldifferencesinthechoiceofcriteriaforspeciesrecognition(deQueiroz,2005a;Markolfetal.,2011).Inrecentyears,theGeneralLineageConceptofSpecies has been fairly generally adopted in the fieldof primatology (Weisrock et al., 2010;Markolf et al.,2011;Markolfetal.,2013),thecriteriamostoftenusedtoascertainorevaluatetheseparatelyevolvinglineagesegmentsconcerned,beingthosederivedfromthePSC,theGSCortheBSC.

Alivelycontroversysubsistsonthehigherorlowernumbers of species that are delineated by use of thePSC,GSCorBSCcriteriaandontheincidencethatsuch

numbershaveonthepracticeofconservationbiology.Forsympatrictaxa,PSC,GSCandBSCcriteria,whenapplied inacontextofsufficientdata,giveessentiallyidenticalresultsforalargespectrumoforganisms(e.g.Alströmetal.,2003;Grovesetal.,2011;Groves,2011;Gippolitietal.,2012;Groves,2013;Devillersetal.,2013;contraZachosetal.,2013a).Thesameislargelytrueoftheapplicationtomostlyparapatrictaxa,hybridisinginazoneofcontact,ofthePSCandtheBSC,atleastintheformsofthelatteramendedbyAmadonetal.(1992)orCoyneetal.(2004).ItisforallopatrictaxathattheBSCandthePSCleadtoverydifferentappreciations.ThePSCdoesinessenceadmitthatgeographicalisolation,per se,doesseparateevolutionarypathswhiletheBSCinsistson a conviction that intrinsic separation mechanismshaveevolved,ensuringcontinueddistinctnessincaseofreunion,beforeacceptingthatthespeciationprocessisunderway.ThePSCdoes therefore identifyas speciesconsiderablymoreallopatricandinsulartaxathendoestheBSC.This isnotsurprising,since,historically, theBSCwasintroducedwiththeexplicitgoalofdrasticallyreducing the number of bird species that had beenindividualizedinthedustofislandsofthecentralPacific(Mayr,1942).

Theincreaseinthenumberofspecies,identifiedbytheapplicationofthePSCorGSC-inspiredcriteria,hasinduceddoubtsorcriticismsabout theconceptualandoperational validity of their formulation (e.g. Collar,1996;Collar, 1997;Agapow et al., 2004; Isaac et al.,2004a;Isaacetal.,2004b;Mace,2004;Garnettetal.,2007; Tattersall, 2007; Markolf et al., 2011; Zachoset al., 2013b; Zachos et al., 2013c). Some criticismsof thisso-called“taxonomicinflation”proceedfromaconservative reflex.Thus,much of the argumentationof Zachos et al. (2013a) aims at showing that somespeciesidentifiedunderthePSCdonotmeetthecriteriaunderpinningtheBSC,ahardlysurprisingobservation.Many doubts and reservations mainly concern theuseof taxonomy inotherdisciplines.Thequestioningmost relevant to evolutionary science itself is that, asformulatedbyTattersall(2007)“evenclearlydiagnosablepopulationscanbenomorethanephemera,atbestmerelypotentialactorsontheevolutionary...stage”.Thatevendistinctive isolates, which are bound by barriers thatfluctuaterapidlyatanevolutionarytime-scale,mightbesoon reabsorbed is avalid argument, though it hardlyapplies to ones which are separated by barriers thatchange in geological time. That isolates may have alimited life-expectancy is amore general observation,buttheirchancesofsurvivalarenotrelatedtowhetheror not they have been, in Tattersall’s (2007) terms,“historically validated—individuated—by speciation”,apropertyheseemstoequatewiththedevelopmentofpresumedintrinsicisolationmechanisms.

Several critics have argued that the elevation tospecies level, through the application of the PSC


criteria,ofasubstantialnumberofpreviouslyknownpopulations or infraspecific taxa is detrimental toconservation (e.g. Collar, 1996; Isaac et al., 2004a;Garnett et al., 2007; Zachos et al., 2013a; Zachoset al., 2013b; Zachos et al., 2013c). The objectionsofmanyoftheseauthorsseemtoproceedmorefromtheall-too-widespreadacceptancethat“theresourcesavailable for conservation are insufficient to preventthelossofmuchoftheworld’sthreatenedbiodiversity”(Collenetal.,2011)thanfromanecessarilyrelentlesseffort to seek support to augment those resources.AmorepreoccupyingconcernisraisedbyZachosetal.(2013b),thatoffinegeneticdiscriminationshinderingrestoration efforts. Examples of such mishaps exist(e.g.Zinketal.,1995),but theymayequallyhappenin a context of species-level over-lumping or over-splitting, and usually result from genetic rigorismunwittinglyservingthevestedinterestsofeconomicorfinancialgrowth.Grovesetal.(2011),Groves(2012)and Gippoliti et al. (2012) convincingly argue theadvantages to conservation of emphasizing species-leveldiversity.

3.2. Recent species-level taxonomic explosion in genus Lepilemur

Lemurs are a prime subject for the study of theevolutionary and biogeographic mechanisms thathaveledtothehighspeciesrichnessandmegadiversebiota of Madagascar (Martin, 1972; Wilmé et al.,2006; Weisrock et al., 2010). In the last decades,the number of lemur populations that have beenindividualized at species-level has considerablyincreased(Groeneveldetal.,2009;Mittermeieretal.,2010). Genus Lepilemur is one of the clades forwhich this explosion has been particularly marked.As lepilemurs are very homogeneous in pelagecoloration and other morphological characters, andtheirvocalisationsandchemicalsignalsarestillverypoorly known. The genus is thus likely to includemany cryptic species (Ravaoarimanana et al., 2003),the term “cryptic species” being taken in the senseof Bickford et al. (2007), as “two or more distinctspecies that are erroneously classified (and hidden)under one species name”.The term is often used inamore restrictive sense todesignate species that aredifficult to distinguish visually, although the animalsthemselves may use quite different signals, auditiveorolfactive for instance, so that theirdifferencesare“cryptic” only to humans. In 1977, genusLepilemurwas thought to include seven species, one of whichwas polytypic (Petter et al., 1977). Since 2001, thetaxonomy of the genus has been frequently revised,mostlythroughuseofconstantlyimprovingmoleculartechniques,anincreasinglypowerfulandvaluabletoolfor thedetectionof cryptic species (Ravaoarimanana

et al., 2003; Andriaholinirina et al., 2006; Louiset al., 2006; Bickford et al., 2007; Groves, 2011).In2001,oneof the subspeciesof themostnortherlyLepilemur, L. septentrionalis, was raised to specieslevel as L. ankaranensis, after identification of thekaryotypes(Rumpleretal.,2001).In2006,threenewspecies were proposed: L. aeeclis, L. randrianasoli,L. sahamalazensis (Andriaholinirina et al., 2006). Inthe same year, Louis et al. (2006) identified 11newspecies,L. fleuretae,L. saeli,L. betsileo,L. wrightae,L. jamesorum, L. ahmansonorum, L. hubbardorum,L. pettri, L. grewcockorum, L. tymerlachsonorumandL. milanoiin,on thebasisofmitochondrialDNA(D-loop,12sRNA)analysis,andRabarivolaetal.(2006)definedL. mittermeierionthebasisofkaryotipicandmtDNAcriteria. In2007,L. ottoandL. manasamodywere described (Craul et al., 2007); the latter washowever later synonymized with L. grewcockorum(Zinner et al., 2007). Finally, L. scottorum andL. hollandorumweredescribedin2008and2009(Leietal.,2008;Ramaromilantoetal.,2009).Thus,atotalof 26species of Lepilemur are currently recognised(Mittermeieretal.,2010;Mittermeier,2013).

As for other groups of organisms that displaysuchatrend,and,notably,for lemursingeneral, thismultiplication (by more than 3 in 10years) of thenumberofrecognizedspeciesofLepilemurhassparkedadebateonwhetherthisincreasereflectsthebiologicalreality or a biased taxonomic subdivision (Tattersall,2007;Groeneveldetal.,2009;Weisrocketal.,2010;Markolfetal.,2011;Thieleetal.,2013).Thus,Tattersall(2007)asksif“thisrecentincreaseofrecognisedlemurspecies[is]duetopreviousunnoticedcrypticdiversity,ortotaxonomicinflation?”.Althoughvalidargumentshave been advanced on both sides of the “inflation”controversy,atleasttheassertionthattheincreaseinthenumberofspecies-leveltaxaiscausedbytherecoursetocriteriainspiredbythePhylogeneticSpeciesConceptis, in thecaseofLepilemur,unfounded.Manyof therecentlydescribedspecies(e.g. Louisetal.,2006)havebeenidentifiedthroughanalysisofmitochondrialDNAin rathersmallsamplesandrelianceon thresholds ingeneticdistancetoascertainspeciesstatus(Tattersall,2007;Markolfetal.,2011).Thisapproachconstitutesa fairly restrictive usage of criteria derived from theGenetic Species Concept, and does not guaranteethat the entities circumscribed meet the criteria thatdefine phylogenetic species, genetic independenceand diagnosability (e.g. Groves, 2011). DifferencesinmtDNAofsmallsamplesindicatedistinctmaternallineages,butdonotprecludemale-mediatedgeneflow,ancestral polymorphism or delays in lineage sorting.Diagnosabilityisnotachievedifitcannotbeshownthatintertaxondifferencesexceed intrataxonvariability,aconditionthatisdifficulttomeetwithsmallsamples.One can however recognize, as Groves (2011), that


“theuseofGSC-inspiredconceptshasbeenenormouslyvaluable in uncovering cryptic diversity in nocturnalMalagasylemurs”andthat,inparticular,thecollectingofmitochondrialsequencedatafortheidentificationofphylogeneticrelationshipswithinthegenusLepilemurhas helped to solve systematic and taxonomic issues(Andriaholinirina et al., 2006). Since the increase inresearcheffortandthefactthatremoteforestshavebeenvisitedmakethedetectionofpreviouslycrypticspeciespredictable(Groeneveldetal.,2009;Mittermeieretal.,2010;Markolfetal.,2011),itappearsbesttoapplytheprincipleofprecaution,andtreattheentitiesidentifiedasspeciesuntil,orunless,suchanhypothesisisfalsified.Thecollectionofecological,geographical,ethological,morphological and molecular data concerning morecharacters and much larger samples of Lepilemurpopulationsareclearlyneededtocomfortorinfirmtheinferences drawn frommitochondrial DNA analyses.Studies aimed at evaluating the congruence in thedistributionofseveralcharactersandtheirconvergencein defining species-level taxa have been conductedfor several other genera, in particular Cheirogaleus(Groeneveldetal.,2009;Thieleetal.,2013),Microcebus(Weisrocketal.,2010;Rasoloarisonetal.,2013)andEulemur (Markolf et al., 2013).Theymostly confirmthe divisions detected through mtDNA analysis, orincreasetheirnumber.Theyfindnosignofunwarranted“taxonomic inflation”.Partial investigationsongenusLepilemur yield similar results (Méndez-Cárdenasetal.,2009),butmoreresearchremainsnecessary.

4. CONCLUSION

This review underlines the biodiversity richness andhigh endemism of Madagascar (Myers et al., 2000;Irwinetal.,2010).Thesecharacteristics,whichspringfromlongisolation,lowratesofcolonizationanduniquenaturalhistory,maketheislandaperfectenvironmentfor studying species diversification (Vences et al.,2009).Themammalian faunaofMadagascarconsistsmainlyoflemurianprimates(Lemuroidea)andmodelsand theories of mechanisms of speciation have beenfrequentlydevelopedonlemurs(Ganzhornetal.,2006;Wilméetal.,2006;Vencesetal.,2009).Threecurrentbiogeographicalmodelsdevelopedtoexplainthehighdiversity of Malagasy primates mainly differ in thenumberofbiogeographicalzones recognised (Martin,1972;Wilméetal.,2006a;Wilméetal.,2006b;Crauletal.,2009).Allthreeattributethehighlevelofendemismtothehydrographicsystemanditshistoricalvariations.The refinements incorporated by successive modelsover theyearshave resulted in the identificationof agrowing number of biogeographical areas (Martin,1972; Wilmé et al., 2006a; Wilmé et al., 2006b;Craul et al., 2009). In the context of these models,

thebiogeographyanddistributionofgenusLepilemurhas been most precisely analyzed in northwesternMadagascar(Rumpleretal.,2001;Andriaholinirinaetal., 2006;Louis et al., 2006;Craul et al., 2007).The“largerivermodel”defineseight“Inter-River-Systems”andseemsparticularlypertinent toexplainLepilemurdistribution(Crauletal.,2007).Thenumberofspecies-leveltaxarecognizedintheinfra-orderLemuriformes,andingenusLepilemurinparticular,hasundergoneaconsiderable recent increase. This trend, shared withanumberofothergroupsoforganisms,isthesubjectof a continuing debate on whether it reflects theuncoveringofpreviouslyundetected(cryptic)diversityor constitutes an artefact attributable to speciesconcepts, criteria for species identification or faultyapplication of these criteria. In the case of lemurs,doubts on the reality of the proposed diversity arekindledbythefrequentrecourse,foritsdetection,toasinglecriterion,thegeneticdistancemeasuredintermsofmitochondrialDNA,andthesmallsamplesusedtoassessthisparameter(Tattersall,2007;Markolfetal.,2011).However,studiesconductedonseveralgenera,specificallydesigned to test, throughconsiderationofseveral characters, the validity of the mtDNA-basedconclusions,haveconfirmedthem.Preliminaryresultson Lepilemur (e.g. Méndez-Cárdenas et al., 2009)suggest the samemayapply in thisgenus.Acceptingthe 26presently described species is, thus, a validworkinghypothesistoinitiatecruciallyneededfurtherstudies. Most of these species are threatened withextinction because of forest destruction and hunting(Méndez-Cárdenasetal.,2008;Mittermeieretal.,2010;Randrianambininaetal.,2010).Assportivelemursarenocturnalanddifficulttodetectandarduoustofollowin thewild, precise estimations of population ranges,sizes, densities and requirements are quite difficult(Méndez-Cárdenas et al., 2008; Randrianambininaetal.,2010).Nevertheless,itisevidentthatLepilemurpopulations, restricted in range and fully forest-dependent,haveahigh-riskofextinction.Therateofdeforestationandforestdegradation inMadagascar isextremelyhigh.Theimpactofsuchathreat,notonlyfor lepilemurs, but for all forest-dependent species issuchthatmeasurestopreventfurtherdestructionmustbeurgentlyimplemented.Todevelopsuchconservationstrategieswiththesupportoflocalcommunities,moredataarestillrequired.Additionalinformationonrangeboundaries,onpopulationdensities,onminimumviablepopulations,andonminimumsizeofforestpatchesarevitallyneededforallLepilemur.

Acknowledgements

ThisworkisessentiallyfundedbyFNRS-FRIA.TheauthorswishtothankJeanDevillers-Terschurenfor therevisionofthemanuscript.


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