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  • Print publication year: 2016
  • Online publication date: March 2016

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

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

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.

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The Dwarf and Mouse Lemurs of Madagascar
  • Online ISBN: 9781139871822
  • Book DOI: https://doi.org/10.1017/CBO9781139871822
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Abbott, R, Albach, D, Arntzen, JW, et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26:229–246.
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.
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.
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.
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.
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.
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.
Dammhahn, M, Kappeler, PM. 2005. Social system of Microcebus berthae, the world's smallest primate. International Journal of Primatology 26:407–435.
Dammhahn, M, Kappeler, P. 2008a. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology 29:1567–1589.
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.
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.
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.
Queiroz, K de. 2007. Species concepts and species delimitation. Systematic Biology 56:879–886.
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.
Felsenstein, J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27:401–410.
Genin, F. 2008. Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. International Journal of Primatology 29:303–321.
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.
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.
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.
Groves, CP. 2000. The genus Cheirogaleus: unrecognized biodiversity in dwarf lemurs. International Journal of Primatology 21:943–962.
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.
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.
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.
Hillis, DM. 1996. Inferring complex phylogenies. Nature 383:130–131.
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.
Huelsenbeck, JP. 1997. Is the Felsenstein zone a fly trap?Systematic Biology 46:69–74.
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.
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.
Knowles, LL, Carstens, BC. 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56:887–895.
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.
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.
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.
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.
Markolf, M, Brameier, M, Kappeler, PM. 2011. On species delimitation: yet another lemur species or just genetic variation?BMC Evolutionary Biology 11:216.
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.
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.
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.
Moore, WS. 1995. Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726.
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.
Ortmann, S, Heldmaier, G, Schmid, J, Ganzhorn, JU. 1997. Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84:28–32.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Rumpler, Y, Albignac, R. 1972. Cytogenetic study of the endemic Malagasy lemurs subfamily Cheirogaleinae Gregory 1915. American Journal of Physical Anthropology 38:261–264.
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.
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.
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.
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.
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.
Schmid, J, Kappeler, PM. 1994. Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Folia Primatologica 63:162–170.
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.
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.
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.
Seehausen, O, Butlin, RK, Keller, I, et al. 2014. Genomics and the origin of species. Nature Reviews Genetics 15:176–192.
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.
Shaffer, HB, Thomson, RC. 2007. Delimiting species in recent radiations. Systematic Biology 56:896–906.
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.
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.
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.
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.
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.
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.
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.
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.
Weisrock, DW, Rasoloarison, RM, Fiorentino, I, et al. 2010. Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. PLoS ONE 5:e9883.
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.
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.
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.
Yoder, AD. 2013. The lemur revolution starts now: the genomic coming of age for a nonmodel organism. Molecular Phylogenetics and Evolution 66:442–452.
Yoder, AD. 2014. Gene flow happens. Evolutionary Anthropology 23:15–17.
Yoder, AD, Yang, Z. 2004. Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Molecular Ecology 13:757–773.
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.
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.
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.
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.
Zimmermann, E, Radespiel, U. 2014. Species concepts, diversity, and evolution in primates: lessons to be learned from mouse lemurs. Evolutionary Anthropology 23:11–14.
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.