[en] Madagascar is one of the highest biodiversity hotspots on the planet; however, it is also one of the most heavily impacted countries in the world in terms of forest degradation and general habitat destruction. Genus Lepilemur, in family Lepilemuridae, is a genus of small, nocturnal, exclusively arboreal Malagasy folivores. All species in the genus have small ranges of distribution. Fully forest-dependent, they have a high risk of extinction. Various models and theories of speciation mechanisms have been developed for the fauna and flora of Madagascar. For instance, in the northwestern part of the island, some authors used Lepilemur spp. to test two existing models of distribution: the “Martin model” and “Wilmé model”.
Regarding the impact of forest destruction and habitat degradation in Madagascar, conservation strategies for Lepilemur need to be put in place. This paper gives an overview of the current knowledge of the genus Lepilemur and examines speciation for Malagasy lemurs. The understanding of species distribution within biodiversity hotspots is important to identify target for conservation. Therefore, we summarize and compare three biogeography models related to lemurs distribution in order to understand the reasons behind the high diversity (26 species in total) among the genus Lepilemur. Particular attention is also given to the concept of species regarding biodiversity issues and the taxonomic explosion in genus Lepilemur.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Wilmet, Leslie ; Université de Liège - ULiège > Forêts, Nature et Paysage > Laboratoire de Foresterie des régions trop. et subtropicales
Schwitzer, Christoph
Devillers, Pierre
Beudels-Jamar, Roseline C.
Vermeulen, Cédric ; Université de Liège - ULiège > Forêts, Nature et Paysage > Laboratoire de Foresterie des régions trop. et subtropicales
Language :
English
Title :
Speciation in Malagasy lemurs: a review of the cryptic diversity in genus Lepilemur
Publication date :
December 2014
Journal title :
Biotechnologie, Agronomie, Société et Environnement
ISSN :
1370-6233
eISSN :
1780-4507
Publisher :
Presses Agronomiques de Gembloux, Gembloux, Belgium
Agapow P.-M. et al., 2004. The impact of species concept on biodiversity studies. Quaterly Rev. Biol., 79, 161-179.
Alström P., 2002. Species limits and systematics in some passerine birds. Comprehensive summaries of Uppsala dissertations from the Faculty of Science and Technology, 726, 1-31.
Alström P. & Mild K., 2003. Pipits and wagtails of Europe, Asia and North America. Identification and systematics. London: Christopher Helm.
Amadon D. & Short L.L., 1992. Taxonomy of lower categories - suggested guidelines. Bull. B.O.C., Centenary Suppl. 112a, 11-38.
Andriaholinirina N. et al., 2006. Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evol. Biol., 6, 17.
Ayeres J.M. & Clutton-Brock T.H., 1992. River boundaries and species range size in Amazonian primates. Am. Nat., 140(3), 531-537.
Baker R.J. & Bradley R.D., 2006. Speciation in mammals and the Genetic Species Concept. J. Mammalogy, 87, 643-662.
Bickford D. et al., 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol., 22(3), 148-155.
Bradley R.D. & Baker R.J., 2001. A test of the Genetic Species Concept: cytochrome-b sequences and mammals. J. Mammalogy, 82, 960-973.
Collar N.J., 1996. Species concepts and conservation: a response to Hazevoet. Bird Conserv. Int., 6, 197-200.
Collar N.J., 1997. Taxonomy and conservation: chicken and egg. Bull. Br. Ornithology Club, 117, 122-136.
Collen B. et al., 2011. Investing in evolutionary history: implementing a phylogenetic approach for mammal conservation. Philos. Trans. R. Soc. London, Ser. B, 366, 2611-2622.
Colquhoun I.C., 2006. Predation and cathemerality. Comparing the impact of predators on the activity patterns of lemurids and ceboids. Folia Primatologica (Basel), 77(1-2), 143-165.
Cotterill F.P.D. et al., 2014. Why one century of phenetics is enough: response to “are there really twice as many bovid species as we thought ?” Syst. Biol., 63(5), 819-832.
Cracraft J., 1983. Species concepts and speciation analysis. Curr. Ornithology, 1, 159-187.
Cracraft J., 1987. Species concepts and the ontology of evolution. Biol. Philosophy, 2, 63-80.
Cracraft J., 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D. & Endler J.A., eds. Speciation and its consequences. Sunderland, MA, USA: Sinauer Associates, Inc.
Craul M. et al., 2007. Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species. BMC Evol. Biol., 7(83).
Craul M. et al., 2009. Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biol. Conserv., 142, 2862-2871.
de Queiroz K., 1998. The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard D.J. & Berlocher S.H., eds. Endless forms: species and speciation. Oxford, UK: Oxford University Press, 57-75.
de Queiroz K., 1999. The general lineage concept of species and the defining properties of the species category. In: Wilson R.A., ed. Species: New interdisciplinary essays. Cambridge, MA, USA: MIT Press, 49-89.
de Queiroz K., 2005a. Ernst Mayr and the modern concept of species.Chapter 13. In: Hey J., Fitch W.M. & Ayala F.J., eds. Systematics and the origin of species: on Ernst Mayr’s 100th Anniversary. Washington: National Academies Press, 243-263.
de Queiroz K., 2005b. A unified species concept and its consequences for the future of taxonomy. Proc. California Acad. Sci., 56(Suppl.1)(18), 196-215.
de Queiroz K., 2005c. Different species problems and their resolution. BioEssays, 27, 1263-1269.
de Queiroz K., 2007. Species concepts and species delimitation. Syst. Biol., 56, 879-886.
Devillers P. & Devillers-Terschuren J., 2013. Orchidées et concepts modernes de l’espèce. Naturalistes Belg., 94(Orchid. 26), 61-74.
Donoghue M.J., 1985. A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist, 88, 172-181.
Fahrig L., 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst., 34, 487-515.
Ganzhorn J.U. et al., 2000. Effects of fragmentation and assessing minimum viable population of lemurs in Madagascar. Bonner Zool. Monographien, 46, 265-272.
Ganzhorn J.U., Goodman S.M., Nash S. & Thalmann U., 2006. Lemur biogeography. Primate biogeography. In: Lehman S.M. & Fleagle J.G., eds. Primate biogeography. Developments in primatology: Progress and prospects. New York, USA: Springer, 229-254.
Garnett S.T. & Christidis L., 2007. Implications of changing species definitions for conservation purposes. Bird Conserv. Int., 17, 187-195
Gippoliti S. & Groves C.P., 2012. “Taxonomic inflation” in the historical context of mammalogy and conservation. Hystrix, 23, 8-11.
Gippoliti S., Cotterill F.P.D. & Groves C.P., 2013. Mammal taxonomy without taxonomists: a reply to Zachos and Lovari. Hystrix, 24, 145-147.
Goodman M.S. & Ganzhorn J.U., 2004. Biogeography of lemurs in the humid forests of Madagascar: the role of elevation distribution and rivers. J. Biogeogr., 31, 47-55.
Goodman M.S. & Benstead J.P., 2005. Update estimates of biotic diversity and endemism for Madagascar. Oryx, 39, 73-77.
Graham C.H., Moritz C. & Williams S.E., 2005. Habitat history improves prediction of biodiversity in rainforest fauna. Proc. Natl. Acad. Sci. U.S.A., 103, 632-636.
Groeneveld L.F. et al., 2009. Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol. Biol., 9, 30.
Groves C.P., 2005. Order primates. In: Wilson D.E. & Reeder D.M. Mammal species of the world: a taxonomic and geographic reference. Baltimore, MD, USA: Johns Hopkins University Press, 111-184.
Groves C., 2011. Introduction to primate taxonomy and species concepts. In: Rowe N. & Myers M., eds. All the world’s primates. Charlestown, RI, USA: Primate Conservation Inc.
Groves C.P., 2012. Species concepts in primates. Am. J. Primatology, 74, 687-691.
Groves C.P., 2013. The nature of species: A rejoinder to Zachos et al. Mammalian Biol., 78, 7-9.
Groves C. & Grubb P., 2011. Ungulate taxonomy. Baltimore, MD, USA: Johns Hopkins University Press.
Harper G.J. et al., 2007. Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv., 34, 1-9.
Irwin M.T. et al., 2010. Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol. Conserv., 143, 2351-2362.
Isaac N.J.B., Mallet J. & Mace G.M., 2004a. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol. Evol., 19, 464-469.
Isaac N.J.B. & Purvis A., 2004b. The ‘species problem’ and testing macroevolutionary hypotheses. Divers. Distrib., 10, 275-281.
Lehman S.M., 2002. Distribution and diversity of primates in Guyana: species-area relationships and riverine barriers. Int. J. Primatol., 25(1), 73-95.
Lei R. et al., 2008. Nocturnal lemur diversity at Masoala National Park. Spec. Publ. Mus. Texas Tech Univ., 53, 1-41.
Louis E.E. Jr. et al., 2006. Molecular and morphological analyses of the sportive lemurs (Family Megaladapideae: Genus Lepilemur) reveals 11 previously unrecognized species. Spec. Publ. Mus. Texas Tech Univ., 49, 1-47.
Mace G.M., 2004. The role of taxonomy in species conservation. Philos. Trans. R. Soc. London, Ser. B, 359, 711-719.
Markolf M., Brameier M. & Kappeler P.M., 2011. On species delimitation: yet another lemur species or just genetic variation? BMC Evol. Biol., 11, 216.
Markolf M. et al., 2013. True lemurs…true species - species delimitation using multiple data sources in the brown lemur complex. BMC Evol. Biol., 13, 233.
Martin R.D., 1972. Adaptive radiation and behavior of the Malagasy lemurs. Philos. Trans. R. Soc. London., Ser. B., 246, 295-352.
Mayr E., 1942. Systematics and the origin of species. New York, USA: Columbia University Press.
Mayr E., 1963. Animal species and evolution. Cambridge, UK: Harvard University Press.
Mayr E., 1969. Principles of systematic zoology. New York, USA: McGraw-Hill.
Méndez-Cárdenas M. et al., 2008. Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation. Am. J. Primatology, 70, 1-11.
Méndez-Cárdenas M. & Zimmermann E., 2009. Duetting - A mechanism to strengthen pair bonds in a dispersed pair-living primate (Lepilemur edwardsi)? Am. J. Phys. Anthropol., 139, 523-532.
Mittermeier R.A., 2013. Introduction. In: Mittermeier R.A., Rylands A.B. & Wilson D.E., eds. Handbook of the mammals of the world. 3. Primates. Barcelona, Spain: Lynx Editions, 13-26.
Mittermeier R.A. et al., 2010. Lemurs of Madagascar. 3d ed. Washington: Conservation International.
Myers N. et al., 2000. Biodiversity hotspots for conservation priorities. Nature, 403, 853-858.
Olivieri G., Craul M. & Radespiel U., 2005. Inventaires des lémuriens dans 15 fragments de forêt de la province de Mahajanga. Lemur News, 10, 11-16.
Olivieri G. et al., 2007. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol. Phylogenet. Evol., 43, 309-327.
Pastorini J., Thalmann U. & Martin R.D., 2003. A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc. Natl. Acad. Sci. U.S.A., 100, 5879-5884.
Paterson H.E.H., 1978. More evidence against speciation by reinforcement. S. Afr. J. Sci., 74, 369-371.
Paterson H.E.H., 1985. The recognition concept of species. In: Vrba E.S., ed. Species and speciation. Transvaal Museum Monograph, 4. Pretoria: Transvaal Museum.
Petter J.J., Albignac R. & Rumpler Y., 1977. Mammifères lémuriens (Primates Prosimiens). Faune de Madagascar, 44. Paris: ORSTOM/CNRS.
Rabarivola C. et al., 2006. Cytogenetic and molecular characteristics of a new species of sportive lemur from northern Madagascar. Lemur News, 11, 45-49.
Ramaromilanto B. et al., 2009. Sportive lemur diversity at Mananara-Nord Biosphere Reserve, Madagascar. Occasional Pap. Mus. Texas Tech Univ., 286, 1-22.
Randrianambinina B. et al., 2007. Seasonality in reproduction of Lepilemur edwardsi. Int. J. Primatology, 28, 783-790.
Randrianambinina B. et al., 2010. Abundance and conservation status of two newly described lemur species in northwestern Madagascar (Microcebus danfossi, Lepilemur grewcockorum). Madagascar Conserv. Dev., 5(2), 95-102.
Rasoloarison R.M. et al., 2013. Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from eastern Madagascar. Int. J. Primatology, 34, 455-469.
Ravaoarimanana I.B., Tiedemann R., Montagnon D. & Rumpler Y., 2003. Molecular and cytogenetic evidence for cryptic speciation within a rare endemic Malagasy lemur, the Northern Sportive Lemur (Lepilemur septentrionalis). Mol. Phylogenet. Evol., 31, 440-448.
Rogers H.M., Glew L., Honzák M. & Hudson M.D., 2010. Prioritizing key biodiversity areas in Madagascar by including data on human pressure and ecosystem services. Landscape Urban Plann., 96, 48-56.
Rumpler Y., Ravoarimanana B., Hauwy M. & Water S., 2001. Cytogenetic arguments in favour of taxonomic revision Lepilemur septentrionalis. Folia Primatologica, 72, 308-315.
Schmid J. & Ganzhorn J., 1996. Resting metabolic rates of Lepilemur mustelinus ruficaudatus. Am. J. Primatology, 38, 169-174.
Schneider N., Chikhi L., Currat M. & Radespiel U., 2010. Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evol. Biol., 10, 105.
Schwitzer C. et al., 2013a. Lemurs of Madagascar: a strategy for their conservation 2013-2016. Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International.
Schwitzer C., Mittermeier R.A., Louis E.E. Jr. & Richardson M.C., 2013b. Family Lepilemuridae (sportive lemurs). In: Mittermeier R.A., Rylands A.B. & Wilson D.E., eds. Handbook of the mammals of the world. 3. Primates. Barcelona, Spain: Lynx Editions, 66-88.
Seiler M., 2012. The impact of habitat degradation and fragmentation on ecology and behaviour of the Sahamalaza sportive lemur, Lepilemur sahamalazensis, in Northwest-Madagascar. PhD thesis: Bristol University, Bristol (England).
Simpson G.G., 1961. Principles of animal taxonomy. New York, USA: Columbia University Press.
Tattersall I., 1982. The primates of Madagascar. New York, USA: Columbia University Press.
Tattersall I., 2007. Madagascar’s lemurs: cryptic diversity or taxonomic inflation? Evol. Anthropol., 16, 12-23.
Thalmann U., 2001. Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. Int. J. Primatology, 22(2), 287-324.
Thiele D., Razafimahatratra E. & Hapke A., 2013. Discrepant partitioning of genetic diversity in mouse lemurs and dwarf lemurs – Biological reality or taxonomic bias? Mol. Phylogenet. Evol., 69, 593-609.
Vences M., Wollenberg K.C., Vieites D.R. & Lees D.C., 2009. Madagascar as a model region of species diversification. Trends Ecol. Evol., 24(8), 456-465.
Warren R.D. & Cromton R.H., 1998. Diet, body size and the energy costs of locomotion in saltatory primates. Folia Primatologica, 69, 86-100.
Weisrock D.W. et al., 2010. Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS One, 5(3), e9883.
Wiens J.J. & Donoghue M.J., 2004. Historical biogeography, ecology and species richness. Trends Ecol. Evol., 19(12), 639-644.
Wiley E.O., 1978. The evolutionary species concept reconsidered. Syst. Zool., 27, 17-26.
Wiley E.O., 1981. Remarks on Willis’ species concept. Syst. Zool., 30, 86-87.
Wilkins J., 2008. Species concepts in modern literature: summary of 26 species concepts. Addendum to Wilkins, J. 2006. Species, kinds and evolution. Rep. Natl. Center Sci. Educ., 26(4), 36-45.
Wilmé L., Goodman M.S. & Ganzhorn J.U., 2006a. Biogeographic evolution of Madagascar’s microendemic biota. Science, 312, 1063-1065.
Wilmé L. & Callmander M.W., 2006b. Les populations reliques de primates: les propithèques. Lemur News, 11, 24-31.
Yoder A.D. & Heckman K., 2006. Mouse lemurs phylogeography revises a model of ecogeographic constraint in Madagascar. In: Fleagle J. & Lehman S.M., eds. Primate biogeography: Progress and prospects. New York, USA: Kluwer, 255-268.
Zachos F.E. et al., 2013a. Species inflation and taxonomic artefacts – A critical comment on recent trends in mammalian classification. Mamm. Biol., 78, 1-6.
Zachos F.E. et al., 2013b. Species splitting puts conservation at risk. Nature, 494, 35.
Zachos F.E. & Lovari S., 2013c. Taxonomic inflation and the poverty of the Phylogenetic Species Concept - a reply to Gippoliti and Groves. Hystrix, 24, 142-144.
Zink R.M. & Kale H.W., 1995. Conservation genetics of the extinct dusky seaside sparrow Ammodramus maritimus nigrescens. Biol. Conserv., 74, 69-71.
Zinner D. et al., 2003. Social organization of Lepilemur ruficaudatus. Int. J. Primatology, 24(4), 869-888.
Zinner D. et al., 2007. Disputed taxonomy classification of sportive lemurs (Lepilemur) in NW Madagascar. Lemur News, 12, 53-56.
