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1 - Cheirogaleid diversity and evolution: big questions about small primates

from Part I - Cheirogaleidae: evolution, taxonomy, and genetics

Published online by Cambridge University Press:  05 March 2016

Anne D. Yoder
Affiliation:
Duke University, USA
David W. Weisrock
Affiliation:
University of Kentucky, USA
Rodin M. Rasoloarison
Affiliation:
Université d'Antananarivo, Madagascar
Peter M. Kappeler
Affiliation:
Behavioural Ecology & Sociobiology Unit, German Primate Center (DPZ), Germany
Shawn M. Lehman
Affiliation:
University of Toronto
Ute Radespiel
Affiliation:
University of Veterinary Medicine Hannover, Foundation
Elke Zimmermann
Affiliation:
University of Veterinary Medicine Hannover, Foundation
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Summary

Introduction

The family Cheirogaleidae is arguably the most interesting group of primates alive today. Within this single clade, hypothesized to have originated approximately 25–30 Mya, we find the world's smallest living primate (genus Microcebus), one species that went “missing” for more than three decades (genus Allocebus), the only known obligate hibernator within the primates (genus Cheirogaleus), the only primate species that preys upon other members of its phylogenetic family (genus Mirza), and also, a taxonomic system that has exploded within the past two decades. This taxonomic explosion has been decidedly lopsided, however. Whereas the genus Allocebus has remained monotypic, containing the single species A. trichotis since its original description in 1875 (Günther 1875), the genus Microcebus (mouse lemurs) has gone from a two species system as recently as 1993 to one that that now contains more than 20 recognized species. This apparent skew in species-level diversity cries out for further exploration. Is it an artifact of organismal and geographic sampling bias, with certain species and ecosystems preferentially sampled, or is it based in biology, with some branches of the cheirogaleid tree (namely, the mouse lemurs) intrinsically more prone to evolutionary divergence? An exploration of these themes and questions is our goal in this chapter.

The first genus-level phylogeny of the cheirogaleid lemurs was published by Rumpler et al. (1994) and has remained virtually unchanged in the subsequent decades. Using karyotype data and restriction fragment analysis, the authors found strong support for the phylogeny illustrated in Figure 1.1. Notably, Rumpler and Albignac (1972) had long before discovered that the karyotype of Phaner (2n = 46) is quite distinct from that of the other four genera (2n = 66), leading those authors to propose a two-subfamily taxonomy of the Cheirogaleidae, the monotypic Phanerinae (including only the genus Phaner) and the Cheirogaleinae (comprising the four remaining genera). More recent molecular phylogenetic analyses have sampled more densely at the species level and have yielded fresh insights into interspecific relationships within the various genera, while leaving the “skeleton” of the phylogeny unchanged.

Type
Chapter
Information
The Dwarf and Mouse Lemurs of Madagascar
Biology, Behavior and Conservation Biogeography of the Cheirogaleidae
, pp. 3 - 20
Publisher: Cambridge University Press
Print publication year: 2016

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References

Abbott, R, Albach, D, Arntzen, JW, et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26:229–246.Google Scholar
Andriantompohavana, R, Zaonarivelo, JR, Engberg, SE, et al. 2006. Mouse lemurs of north-western Madagascar with a description of a new species at Lokobe Special Reserve. Occasional Papers Museum of Texas Tech University259.Google Scholar
Blair, C, Heckman, KL, Russell, AL, Yoder, AD. 2014. Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species. BMC Evolutionary Biology 14:57.Google Scholar
Bohr, YEMB, Giertz, P, Ratovonamana, YR, Ganzhorn, JU. 2011. Gray-brown mouse lemurs (Microcebus griseorufus) as an example of distributional constraints through increasing desertification. International Journal of Primatology 32:901–913.Google Scholar
Braune, P, Schmidt, S, Zimmermann, E. 2005. Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis): the role of olfactory and acoustic signals. Behavioral Ecology and Sociobiology 58:587–596.Google Scholar
Braune, P, Schmidt, S, Zimmermann, E. 2008. Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.). BMC Biology 6:1–10.Google Scholar
Crowley, BE, Rasoazanabary, E, Godfrey, LR. 2014. Stable isotopes complement focal individual observations and confirm dietary variability in reddish–gray mouse lemurs (Microcebus griseorufus) from southwestern Madagascar. American Journal of Physical Anthropology 155:77–90.Google Scholar
Dammhahn, M, Kappeler, PM. 2005. Social system of Microcebus berthae, the world's smallest primate. International Journal of Primatology 26:407–435.Google Scholar
Dammhahn, M, Kappeler, P. 2008a. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology 29:1567–1589.Google Scholar
Dammhahn, M, Kappeler, PM. 2008b. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment. Oecologia 157:473–483.Google Scholar
Dammhahn, M, Kappeler, PM. 2010. Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): new insights from stable isotopes. American Journal of Physical Anthropology 141:181–189.Google Scholar
Dammhahn, M, Kappeler, PM. 2014. Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a Malagasy primate community. American Journal of Physical Anthropology 153:249–259.Google Scholar
Queiroz, K de. 2007. Species concepts and species delimitation. Systematic Biology 56:879–886.Google Scholar
Eichmueller, P, Thoren, S, Radespiel, U. 2013. The lack of female dominance in golden-brown mouse lemurs suggests alternative routes in lemur social evolution. American Journal of Physical Anthropology 150:158–164.Google Scholar
Felsenstein, J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27:401–410.Google Scholar
Genin, F. 2008. Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. International Journal of Primatology 29:303–321.Google Scholar
Gligor, M, Ganzhorn, JU, Rakotondravony, D, et al. 2009. Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar. Molecular Ecology 18:520–533.Google Scholar
Groeneveld, LF, Weisrock, DW, Rasoloarison, RM, Yoder, AD, Kappeler, PM. 2009. Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evolutionary Biology 9:30.Google Scholar
Groeneveld, LF, Blanco, MB, Raharison, JL, et al. 2010. MtDNA and nDNA corroborate existence of sympatric dwarf lemur species at Tsinjoarivo, eastern Madagascar. Molecular Phylogenetics and Evolution 55:833–845.Google Scholar
Groves, CP. 2000. The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. International Journal of Primatology 21:943–962.Google Scholar
Günther, A. 1875. Notes on some mammals from Madagascar. Proceedings of the Zoological Society of London 1875, 78–80.
Hapke, A, Gligor, M, Rakotondranary, SJ, Rosenkranz, D, Zupke, O. 2011. Hybridization of mouse lemurs: different patterns under different ecological conditions. BMC Evolutionary Biology 11:297.Google Scholar
Heckman, KL, Rasoazanabary, E, Machlin, E, Godfrey, LR, Yoder, AD. 2006. Incongruence between genetic and morphological diversity in Microcebus griseorufus of Beza Mahafaly. BMC Evolutionary Biology 6:98.Google Scholar
Heckman, KL, Mariani, CL, Rasoloarison, R, Yoder, AD. 2007. Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). Molecular Phylogenetics and Evolution 43:353–367.Google Scholar
Hillis, DM. 1996. Inferring complex phylogenies. Nature 383:130–131.Google Scholar
Hohenbrink, P, Radespiel, U, Mundy, NI. 2012. Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs. Molecular Biology and Evolution 29:3807–3816.Google Scholar
Huelsenbeck, JP. 1997. Is the Felsenstein zone a fly trap?Systematic Biology 46:69–74.Google Scholar
Jones, G. 1997. Acoustic signals and speciation: the roles of natural and sexual selection in the evolution of cryptic species. Advances in the Study of Behavior 26:317–354.Google Scholar
Kappeler, PM, Rasoloarison, RM. 2003. Microcebus, mouse lemurs, Tsidy. In Goodman, SM, Benstead, JP (eds.), The Natural History of Madagascar (pp. 1310–1315). University of Chicago Press, Chicago.
Kappeler, PM, Rasoloarison, R, Razafimanantsoa, L, Walter, L, Roos, C. 2005. Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Report 71:3–26.Google Scholar
Knowles, LL, Carstens, BC. 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56:887–895.Google Scholar
Kobbe, S, Ganzhorn, JU, Dausmann, KH. 2011. Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). Journal of Comparative Physiology B Biochemical Systemic and Environmental Physiology 181:165–173.Google Scholar
Leliveld, LMC, Scheumann, M, Zimmermann, E. 2011. Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus). Journal of the Acoustical Society of America 129:2278–2288.Google Scholar
Louis, EE, Coles, MS, Andriantompohavana, R, et al. 2006. Revision of the mouse lemurs (Microcebus) of eastern Madagascar. International Journal of Primatology 27:347–389.Google Scholar
Louis, EE, Engberg, SE, McGuire, SM, et al. 2008. Rivision of the mouse lemurs, Microcebus (Primates, Lemuriformes), of northern and northwestern Madagascar with descriptions of two new species at Montagne d'Ambre National Park and Antafondro Classified Forest. Primate Conservation 23:19–38.Google Scholar
Markolf, M, Brameier, M, Kappeler, PM. 2011. On species delimitation: yet another lemur species or just genetic variation?BMC Evolutionary Biology 11:216.Google Scholar
Markolf, M, Rakotonirina, H, Fichtel, C, et al. 2013. True lemurs … true species – species delimitation using multiple data sources in the brown lemur complex. BMC Evolutionary Biology 13:233.Google Scholar
Martin, RD. 1972. A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller, 1777). Zeitschrift für Tierpychologie (Suppl 9):43–89.Google Scholar
Masters, JC, Silvestro, D, Génin, F, DelPero, M. 2013. Seeing the wood through the trees: the current state of higher systematics in the Strepsirrhini. Folia Primatologica 84:201–219.Google Scholar
Moore, WS. 1995. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726.Google Scholar
Olivieri, G, Zimmermann, E, Randrianambinina, B, et al. 2007. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution 43:309–327.Google Scholar
Ortmann, S, Heldmaier, G, Schmid, J, Ganzhorn, JU. 1997. Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32.Google Scholar
Radespiel, U, Ehresmann, P, Zimmermann, E. 2003. Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in Northwestern Madagascar. American Journal of Primatology 59:139–151.Google Scholar
Radespiel, U, Reimann, W, Rahelinirina, M, Zimmermann, E. 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. International Journal of Primatology 27:311–321.Google Scholar
Radespiel, U, Olivieri, G, Rasolofoson, DW, et al., 2008. Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. American Journal of Primatology 70:1033–1046.Google Scholar
Radespiel, U, Juric, M, Zimmermann, E. 2009. Sociogenetic structures, dispersal and the risk of inbreeding in a small nocturnal lemur, the golden-brown mouse lemur (Microcebus ravelobensis). Behaviour 146:607–628.Google Scholar
Radespiel, U, Ratsimbazafy, JH, Rasoloharijaona, S, et al. 2012. First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar. Primates 53:157–170.Google Scholar
Rakotondranary, SJ, Ganzhorn, JU. 2011. Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar. Folia Primatologica 82:212–223.Google Scholar
Rakotondranary, SJ, Hapke, A, Ganzhorn, JU. 2011a. Distribution and morphological variation of Microcebus spp. along an environmental gradient in southeastern Madagascar. International Journal of Primatology 32:1037–1057.Google Scholar
Rakotondranary, SJ, Struck, U, Knoblauch, C, Ganzhorn, JU. 2011b. Regional, seasonal and interspecific variation in (15)N and (13)C in sympatric mouse lemurs. Naturwissenschaften 98:909–917.Google Scholar
Rakotondravony, R, Radespiel, U. 2009. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. American Journal of Primatology 71:928–938.Google Scholar
Rasoloarison, RM, Goodman, SM, Ganzhorn, JU. 2000. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology 21:963–1019.Google Scholar
Rasoloarison, RM, Weisrock, DW, Yoder, AD, Rakotondravony, D, Kappeler, PM. 2013. Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from Eastern Madagascar. International Journal of Primatology 34:455–469.Google Scholar
Rendigs, A, Radespiel, U, Wrogemann, D, Zimmermann, E. 2003. Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in northwestern Madagascar. International Journal of Primatology 24:47–64.Google Scholar
Roos, C, Schmitz, J, Zischler, H. 2004. Primate jumping genes elucidate strepsirrhine phylogeny. Proceedings of the National Academy of Sciences of the United States of America 101:10650–10654.Google Scholar
Rumpler, Y, Albignac, R. 1972. Cytogenetic study of the endemic Malagasy lemurs subfamily Cheirogaleinae Gregory 1915. American Journal of Physical Anthropology 38:261–264.Google Scholar
Rumpler, Y, Crovella, S, Montagnon, D. 1994. Systematic relationships among Cheirogaleidae (Primates, Strepsirhini) determined from analysis of highly repeated DNA. Folia Primatologica 63:149–155.Google Scholar
Schäffler, L, Kappeler, P. 2014. Distribution and abundance of the world's smallest primate, Microcebus berthae, in Central Western Madagascar. International Journal of Primatology 35:557–572.Google Scholar
Schäffler, L, Saborowski, J, Kappeler, PM, 2015. Agent-mediated spatial storage effect in heterogeneous habitat stabilizes competitive mouse lemur coexistence in Menabe Central, Western Madagascar. BMC Ecology 15:7. DOI: 10.1186/s12898-015-0040-1.
Scheumann, M, Zimmermann, E, Deichsel, G. 2007. Context-specific calls signal infants' needs in a strepsirrhine primate, the gray mouse lemur (Microcebus murinus). Developmental Psychobiology 49:708–718.Google Scholar
Schliehe-Diecks, S, Eberle, M, Kappeler, PM. 2012. Walk the line – dispersal movements of gray mouse lemurs (Microcebus murinus). Behavioral Ecology and Sociobiology 66:1175–1185.Google Scholar
Schmid, J. 1999. Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. Journal of Mammalogy 80:749–757.Google Scholar
Schmid, J, Kappeler, PM. 1994. Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Folia Primatologica 63:162–170.Google Scholar
Schmid, J, Kappeler, PM. 1998. Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behavioral Ecology and Sociobiology 43:125–132.Google Scholar
Schmid, J, Ruf, T, Heldmaier, G. 2000. Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal of Comparative Physiology B Biochemical Systemic and Environmental Physiology 170:59–68.Google Scholar
Schwab, D, Ganzhorn, JU. 2004. Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogaleids. International Journal of Primatology 25:307–330.Google Scholar
Seehausen, O, Butlin, RK, Keller, I, et al. 2014. Genomics and the origin of species. Nature Reviews Genetics 15:176–192.Google Scholar
Sehen, L, Goetze, D, Rajeriarison, C, et al. 2010. Structural and floristic traits of habitats with differing relative abundance of the lemurs Microcebus murinus and M. ravelobensis in Northwestern Madagascar. Ecotropica 16:15–30.Google Scholar
Shaffer, HB, Thomson, RC. 2007. Delimiting species in recent radiations. Systematic Biology 56:896–906.Google Scholar
Simpson, GG. 1961. Principles of Animal Taxonomy. Columbia University Press, New York.
Sommer, S, Rakotondranary, SJ, Ganzhorn, JU. 2014. Maintaining microendemic primate species along an environmental gradient – parasites as drivers for species differentiation. Ecology and Evolution 4(24):4751–4765.Google Scholar
Springer, MS, Meredith, RW, Gatesy, J, et al. 2012. Macroevolutionary dynamics and historical biogeogrphy of primate diversification inferred from a species supermatrix. PLoS ONE 7:e49521.Google Scholar
Swofford, DL. 1990. PAUP: Phylogenetic Analysis Using Parsimony. Illinois Natural History Survey, Champaign, IL.
Tattersall, I. 2007. Madagascar's lemurs: cryptic diversity or taxonomic inflation?Evolutionary Anthropology 16:12–23.Google Scholar
Terrien, J, Ambid, L, Nibbelink, M, Saint-Charles, A, Aujard, F. 2010a. Non-shivering thermogenesis activation and maintenance in the aging gray mouse lemur (Microcebus murinus). Experimental Gerontology 45:442–448.Google Scholar
Terrien, J, Perret, M, Aujard, F. 2010b. Gender markedly modulates behavioral thermoregulation in a non-human primate species, the mouse lemur (Microcebus murinus). Physiology and Behavior 101:469–473.Google Scholar
Thiele, D, Razafimahatratra, E, Hapke, A. 2013. Discrepant partitioning of genetic diversity in mouse lemurs and dwarf lemurs – biological reality or taxonomic bias?Molecular Phylogenetics and Evolution 69:593–609.Google Scholar
Thoren, S, Linnenbrink, M, Radespiel, U. 2011a. Different competitive potential in two coexisting mouse lemur species in Northwestern Madagascar. American Journal of Physical Anthropology 145:156–162.Google Scholar
Thoren, S, Quietzsch, F, Schwochow, D, et al. 2011b. Seasonal changes in feeding ecology and activity patterns of two sympatric mouse lemur species, the Gray Mouse Lemur (Microcebus murinus) and the Golden-brown Mouse Lemur (M. ravelobensis), in Northwestern Madagascar. International Journal of Primatology 32:566–586.Google Scholar
Weisrock, DW, Rasoloarison, RM, Fiorentino, I, et al. 2010. Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. PLoS ONE 5:e9883.Google Scholar
Weisrock, DW, Smith, SD, Chan, LM, et al. 2012. Concatenation and concordance in the reconstruction of mouse lemur phylogeny: an empirical demonstration of the effect of allele sampling in phylogenetics. Molecular Biology and Evolution 29:1615–1630.Google Scholar
Wiens, JJ, Hollingsworth, BD 2000. War of the iguanas: conflicting molecular and morphological phylogenies and long-branch attraction in iguanid lizards. Systematic Biology 49:143–159.Google Scholar
Yang, ZH, Yoder, AD. 2003. Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Systematic Biology 52:705–716.Google Scholar
Yoder, AD. 2013. The lemur revolution starts now: the genomic coming of age for a nonmodel organism. Molecular Phylogenetics and Evolution 66:442–452.Google Scholar
Yoder, AD. 2014. Gene flow happens. Evolutionary Anthropology 23:15–17.Google Scholar
Yoder, AD, Yang, Z. 2004. Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Molecular Ecology 13:757–773.Google Scholar
Yoder, AD, Rasoloarison, RM, Goodman, SM, et al. 2000. Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Proceedings of the National Academy of Sciences of the United States of America 97:11325–11330.Google Scholar
Yoder, AD, Burns, MM, Genin, F. 2002. Molecular evidence of reproductive isolation in sympatric sibling species of mouse lemurs. International Journal of Primatology 23:1335–1343.Google Scholar
Yoder, AD, Olson, LE, Hanley, C, et al. 2005. A multidimensional approach for detecting species patterns in Malagasy vertebrates. Proceedings of the National Academy of Sciences of the United States of America 102:6587–6594.Google Scholar
Yoder, AD, Chan, LM, Reis, M dos, et al., 2014. Molecular evolutionary characterization of a V1R subfamily unique to strepsirrhine primates. Genome Biology and Evolution 6:213–227.Google Scholar
Zimmermann, E, Radespiel, U. 2014. Species concepts, diversity, and evolution in primates: lessons to be learned from mouse lemurs. Evolutionary Anthropology 23:11–14.Google Scholar
Zimmermann, E, Cepok, S, Rakotoarison, N, Zietemann, V, Radespiel, U. 1998. Sympatric mouse lemurs in north-west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatologica 69, 106–114.Google Scholar

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