Skip to main content Accessibility help
Hostname: page-component-758b78586c-qvhcc Total loading time: 0 Render date: 2023-11-27T15:52:14.385Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "useRatesEcommerce": true } hasContentIssue false

22 - Modeling the origins of primate sociality: social fl exibility and kinship in mouse lemurs (Microcebus spp.)

from Part IV - Cheirogaleidae: sensory ecology, communication, and cognition

Published online by Cambridge University Press:  05 March 2016

Sharon E. Kessler
McGill University, Canada
Ute Radespiel
University of Veterinary Medicine Hannover, Germany
Leanne T. Nash
Arizona State University, USA
Elke Zimmermann
University of Veterinary Medicine Hannover, Germany
Shawn M. Lehman
University of Toronto
Ute Radespiel
University of Veterinary Medicine Hannover, Foundation
Elke Zimmermann
University of Veterinary Medicine Hannover, Foundation
Get access


The dawn of primate social complexity: kin selection in asocial mammals

Since Hamilton's ground-breaking theory of inclusive fitness in 1964, kin-biased behavior has been theorized to have played a crucial role in the evolution of mammalian sociality (Hamilton, 1964; de Waal and Tyack, 2003; Chapais and Berman, 2004). Given the amount of attention given to the topic over the subsequent decades, it is surprising that while group-living and social complexity has evolved multiple times in mammals, we still know very little about how this process occurs (Waser and Jones, 1983; Müller and Thalmann, 2000; de Waal and Tyack, 2003). In this section we review what is known about ancestral mammals and how they were the foundation for the evolution of ancestral primates.

Ancestral mammals are believed to have been asocial, as are many extant mammal species (Waser and Jones, 1983; Müller and Thalmann, 2000). Asocial species forage alone and maintain no relationships outside of the mating and infant-rearing seasons (Charles-Dominique, 1974, 1978; Waser and Jones, 1983; Müller and Thalmann, 2000). Interactions between adults, including adult kin, are marked by avoidance and aggression (Charles-Dominique, 1974; Waser and Jones, 1983; Müller and Thalmann, 2000). This is note-worthy because in many species, females typically disperse shorter distances than males, leading to a spatial clustering of female kin (Waser and Jones, 1983; Stoen et al., 2005; Maher, 2009). For many scientists, it is this spatial clustering of kin which is the first step towards increasing sociality (Waser and Jones, 1983; Perrin and Lehmann, 2001; Kappeler et al., 2002; Lutermann et al., 2006; Meshriy et al., 2011; Messier et al., 2012). The transition to group-living is believed to have occurred through solitary foraging (Müller and Thalmann, 2000). Extant solitary foragers forage alone, but, in contrast to the asocial mammalian ancestors, maintain year-round social networks, communicating with conspecifics via scent-marks and vocalizations (Charles-Dominique, 1974, 1978; Zimmermann, 1990, 1995a, 1995b, 2010; Müller and Thalmann, 2000; Nash, 2004; see also Chapter 21). Individuals may interact affiliatively during their active periods and sometimes sleep in social groups, often consisting of matrilineal kin, during the inactive periods (e.g., Radespiel et al., 2001b; Eberle and Kappeler 2006; for review, see Müller and Thalmann, 2000).

The Dwarf and Mouse Lemurs of Madagascar
Biology, Behavior and Conservation Biogeography of the Cheirogaleidae
, pp. 422 - 446
Publisher: Cambridge University Press
Print publication year: 2016

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Barton, RA. 2006. Primate brain evolution: integrating comparative, neurophysiological, and ethological data. Evolutionary Anthropology 15(6):224–236.Google Scholar
Bearder, SK. 1987. Lorises, bushbabies, and tarsiers: diverse societies in solitary foragers. In Smuts, BB, Cheney, DL, Seyfarth, RM, Wrangham, R, Struhsaker, TT (eds.), Primate Societies (pp. 11–24). University of Chicago Press, Chicago.
Bloch, JI, Boyer, DM. 2002. Grasping primate origins. Science 298(5598):1606–1610.Google Scholar
Bloch, JI, Silcox, MT, Boyer, DM, Sargis, EJ. 2007. New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proceedings of the National Academy of Sciences of the United States of America 104(4):1159–1164.Google Scholar
Braune, P. 2007. Acoustic Variability and its Biological Significance in Nocturnal Lemurs. Gottfried Wilhelm Leibniz Universität Hannover, Hannover.
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(6):587–596.Google Scholar
Broad, KD, Curley, JP, Keverne, EB. 2006. Mother–infant bonding and the evolution of mammalian social relationships. Philosophical Transactions of the Royal Society B Biological Sciences 361(1476):2199–2214.Google Scholar
Cartmill, M. 1972. Arboreal adaptations and the origin of the order Primates. In Tuttle, RH (ed.), The Functional and Evolutionary Biology of Primates (pp. 97–122). Aldine-Atherton, Chicago.
Cartmill, M. 1974. Rethinking primate origins. Science 184(4135):436–443.Google Scholar
Cartmill, M. 1992. New views on primate origins. Evolutionary Anthropology 1:105–111.Google Scholar
Cartmill, M. 2012. Primate origins, human origins, and the end of higher taxa. Evolutionary Anthropology 21(6):208–220.Google Scholar
Chapais, B, Berman, CM (eds.) 2004. Kinship and Behavior in Primates. Oxford University Press, New York.
Charles-Dominique, P. 1974. Aggression and territoriality in nocturnal prosimians. In Holloway, RL (ed.), Primate Aggression, Territoriality, and Xenophobia (pp. 31–48). Academic Press, New York.
Charles-Dominique, P. 1978. Nocturnality and diurnality: an ecological interpretation of these two modes of life by an analysis of the higher vertebrate fauna in tropical forest ecosystems. In Luckett, WP, Szalay, FS (eds.), Phylogeny of the Primates (pp. 69–88). Plenum Press, New York.
Charles-Dominique, P, Martin, RD. 1970. Evolution of lorises and lemurs. Nature 227(5255):257–260.Google Scholar
Charles-Dominique, P, Martin, RD. 1972. Behaviour and Ecology of Nocturnal Prosimians: Field Studies in Gabon and Madagascar. P. Parey, Berlin.
Dammhahn, M, Kappeler, PM. 2005. Social system of Microcebus berthae, the world's smallest primate. International Journal of Primatology 26(2):407–435.Google Scholar
Dammhahn, M, Kappeler, P. 2008a. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology 29(6):1567–1589.Google Scholar
Dammhahn, M, Kappeler, P. 2008b. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment. Oecologia 157(3):473–483.Google Scholar
Dammhahn, M, Kappeler, PM. 2009. Females go where the food is: does the socio-ecological model explain variation in social organisation of solitary foragers?Behavioral Ecology and Sociobiology 63(6):939–952.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(2):181–189.Google Scholar
Dausmann, KH. 2014. Flexible patterns in energy savings: heterothermy in primates. Journal of Zoology 292(2):101–111.Google Scholar
Waal, F de, Tyack, PL (eds.) 2003. Animal Social Complexity: Intelligence, Culture, and Individualized Societies. Harvard University Press, Cambridge.
Dunbar, R. 1998. The social brain hypothesis. Evolutionary Anthropology 6(5):178–190.Google Scholar
Eberle, M, Kappeler, PM. 2002. Mouse lemurs in space and time: a test of the socioecological model. Behavioral Ecology and Sociobiology 51(2):131–139.Google Scholar
Eberle, M, Kappeler, PM. 2004a. Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology 57(1):91–100.Google Scholar
Eberle, M, Kappeler, PM. 2004b. Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behavioral Ecology and Sociobiology 57(1):77–90.Google Scholar
Eberle, M, Kappeler, PM. 2006. Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behavioral Ecology and Sociobiology 60(4):582–588.Google Scholar
Gebo, DL. 2004. A shrew-sized origin for primates. Yearbook of Physical Anthropology 47:40–62.Google Scholar
Génin, F. 2008. Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. International Journal of Primatology 29:303–321.Google Scholar
Génin, F. 2010. Who sleeps with whom? Sleeping association and socio-territoriality in Microcebus griseorufus. Journal of Mammalogy 91(4):942–951.Google Scholar
Ghazanfar, AA. 2013. Multisensory vocal communication in primates and the evolution of rhythmic speech. Behavioral Ecology and Sociobiology 67(9):1441–1448.Google Scholar
Gingerich, PD, Uhen, MD. 1994. Time of origin of primates. Journal of Human Evolution 27(5):443–445.Google Scholar
Hamilton, WD. 1964. The genetical evolution of social behavior. I and II. Journal of Theoretical Biology 7:1–52.Google Scholar
Hatchwell, BJ. 2010. Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116(3):203–216.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(12):3807–3816.Google Scholar
Hohenbrink, P, Mundy, NI, Zimmermann, E, Radespiel, U. 2013. First evidence for functional vomeronasal 2 receptor genes in primates. Biology Letters 9(1):20121006.Google Scholar
Holekamp, KE, Smith, JE, Strelioff, CC, Horn, RC Van, Watts, HE. 2012. Society, demography and genetic structure in the spotted hyena. Molecular Ecology 21(3):613–632.Google Scholar
Jürges, V, Kitzler, J, Zingg, R, Radespiel, U. 2013. First insights into the social organization of Goodman's mouse lemur (Microcebus lehilahytsara) – testing predictions from socio-ecological hypotheses in the Masoala Hall of Zurich Zoo. Folia Primatologica 84:32–48.Google Scholar
Kappeler, P, Rasoloarison, R, Razafimanantsoa, L, Walter, L, Roos, C. 2005. Morphology, behavior and molecular evolution of giant mouse lemurs (Mirza spp.), Gray 1970, with a description of a new species. Primate Report 71:3–26.Google Scholar
Kappeler, PM. 1997. Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biological Reviews of the Cambridge Philosophical Society 72(1):111–151.Google Scholar
Kappeler, PM. 1998. Nests, tree holes, and the evolution of primate life histories. American Journal of Primatology 46(1):7–33.Google Scholar
Kappeler, PM, Schaik, CP van. 2002. Evolution of primate social systems. International Journal of Primatology 23(4):707–740.Google Scholar
Kappeler, PM, Wimmer, B, Zinner, D, Tautz, D. 2002. The hidden matrilineal structure of a solitary lemur: implications for primate social evolution. Proceedings of the Royal Society of London Series B Biological Sciences 269(1502):1755–1763.Google Scholar
Kessler, SE. 2014. Modeling the Origins of Primate Sociality: Kin Recognition in Mouse Lemurs. Arizona State University, Tempe.
Kessler, SE, Scheumann, M, Nash, LT, Zimmermann, E. 2012. Paternal kin recognition in the high frequency/ultrasonic range in a solitary foraging mammal. BMC Ecology 12:26.Google Scholar
Kessler, SE, Radespiel, U, Hasiniaina, A, et al. 2014. Modeling the origins of mammalian sociality: moderate evidence for matrilineal signatures in mouse lemur vocalizations. Frontiers in Zoology 11:14.Google Scholar
Kitzler, J. 2011. Genetische struckturen in der population von Goodman mausmakis in der Masoala Halle, Zoo Zürich. Bachelorarbeit, Gottfried Wilhelm Leibniz Universität Hannover, Hannover.
Komdeur, J, Hatchwell, BJ. 1999. Kin recognition: function and mechanism in avian societies. Trends in Ecology and Evolution 14:237–241.Google Scholar
Kulahci, IG, Drea, CM, Rubenstein, DI, Ghazanfar, AA. 2014. Individual recognition through olfactory–auditory matching in lemurs. Proceedings of the Royal Society B Biological Sciences 281(1784):6.Google Scholar
Lahann, P. 2007. Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. Journal of Zoology 271(1):88–98.Google Scholar
Lahann, P. 2008. Habitat utilization of three sympatric cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. International Journal of Primatology 29(1):117–134.Google Scholar
Lahann, P, Dausmann, KH. 2011. Live fast, die young: flexibility of life history traits in the fat-tailed dwarf lemur (Cheirogaleus medius). Behavioral Ecology and Sociobiology 65(2):381–390.Google Scholar
Lahann, P, Schmid, J, Ganzhorn, JU. 2006. Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule?International Journal of Primatology 27(4):983–999.Google Scholar
Lemelin, P. 1999. Morphological correlates of substrate use in didelphid marsupials: implications for primate origins. Journal of Zoology 247:165–175.Google Scholar
Lutermann, H, Schmelting, B, Radespiel, U, Ehresmann, P, Zimmermann, E. 2006. The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus). Proceedings of the Royal Society B Biological Sciences 273(1600):2527–2533.Google Scholar
Lutermann, H, Verburgt, L, Rendigs, A. 2010. Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs. Animal Behaviour 79(6):1211–1219.Google Scholar
Maher, CR. 2009. Genetic relatedness and space use in a behaviorally flexible species of marmot, the woodchuck (Marmota monax). Behavioral Ecology and Sociobiology 63(6):857–868.Google Scholar
Martin, RD. 1993. Primate origins – plugging the gaps. Nature 363(6426):223–234.Google Scholar
Martin, RD, Soligo, C, Tavare, S. 2007. Primate origins: implications of a cretaceous ancestry. Folia Primatologica 78(5–6):277–296.Google Scholar
Mateo, JM. 2004. Recognition systems and biological organization: the perception component of social recognition. Annales Zoologici Fennici 41(6):729–745.Google Scholar
Mateo, JM. 2010. Self-referent phenotype matching and long-term maintenance of kin recognition. Animal Behaviour 80(5):929–935.Google Scholar
McComb, K, Moss, C, Sayialel, S, Baker, L. 2000. Unusually extensive networks of vocal recognition in African elephants. Animal Behaviour 59(6):1103–1109.Google Scholar
Meshriy, MG, Randall, JA, Parra, L. 2011. Kinship associations of a solitary rodent, Dipodomys ingens, at fluctuating population densities. Animal Behaviour 82(4):643–650.Google Scholar
Messier, GD, Garant, D, Bergeron, P, Reale, D. 2012. Environmental conditions affect spatial genetic structures and dispersal patterns in a solitary rodent. Molecular Ecology 21(21):5363–5373.Google Scholar
Montgomery, SH, Mundy, N. 2013. Parallel espidoes of phyletic dwarfism in callitrichid and cheirogaleid primates. Journal of Evolutionary Biology 26:810–819.Google Scholar
Müller, A, Soligo, C. 2005. Primate sociality in evolutionary context. American Journal of Physical Anthropology 128(2):399–414.Google Scholar
Müller, AE, Thalmann, U. 2000. Origin and evolution of primate social organisation: a reconstruction. Biological Review 75:405–435.Google Scholar
Nash, LT. 2004. Kinship and behavior among nongregarious nocturnal prosimians: what do we really know? In Chapais, B, Berman, CM (eds.), Kinship and Behavior in Primates (pp. 200–222). Oxford University Press, New York.
Nekaris, KAI. 2005. Foraging behaviour of the slender loris (Loris lydekkerianus lydekkerianus): implications for theories of primate origins. Journal of Human Evolution 49(3):289–300.Google Scholar
Nekaris, KAI, Bearder, S. 2011. The strepsirrhine primates of Asia and Mainland Africa: diversity shrouded in darkness. In Campbell, C, Fuentes, A, MacKinnon, K, Bearder, S, Stumpf, R (eds.), Primates in Perspective, 2nd edition. Oxford University Press, Oxford.
Ni, XJ, Wang, YQ, Hu, YM, Li, CK. 2004. A euprimate skull from the early Eocene of China. Nature 427(6969):65–68.Google Scholar
Ni, XJ, Hu, YM, Wang, YQ, Li, CK. 2005. A clue to the Asian origin of euprimates. Anthropological Science 113(1):3–9.Google Scholar
Perret, M. 1998. Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus murinus). Journal of Mammalogy 79(4):1093–1102.Google Scholar
Perrin, N, Lehmann, L. 2001. Is sociality driven by the costs of dispersal or the benefits of philopatry? A role for kin-discrimination mechanisms. American Naturalist 158(5):471–483.Google Scholar
Perry, S. 2011. Social traditions and social learning in capuchin monkeys (Cebus). Philosophical Transactions of the Royal Society B Biological Sciences 366(1567):988–996.Google Scholar
Pfefferle, D, Lambides, AV Ruiz, Widdig, A. 2014. Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: support for acoustic phenotype matching. Proceedings of the Royal Society B 281(1774):20131628.Google Scholar
Radespiel, U. 2006. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In Gould, L, Sauther, ML (eds.), Lemurs: Ecology and Adaptation (pp. 211–234). Springer, New York.
Radespiel, U, Cepok, S, Zietemann, V, Zimmermann, E. 1998. Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology 46(1):77–84.Google Scholar
Radespiel, U, Ehresmann, P, Zimmermann, E. 2001a. Contest versus scramble competition for mates: the composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in northwest Madagascar. Primates 42(3):207–220.Google Scholar
Radespiel, U, Sarikaya, Z, Zimmermann, E, Bruford, MW. 2001b. Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus). Behavioral Ecology and Sociobiology 50(6):493–502.Google Scholar
Radespiel, U, Secco, V Dal, Drogemuller, C, et al. 2002. Sexual selection, multiple mating and paternity in grey mouse lemurs, Microcebus murinus. Animal Behaviour 63:259–268.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(4):139–151.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
Randrianambinina, B. 2001. Contribution à l'étude comparative de l'écoéthologie de deux microcèbes rouges de Madagascar: Microcebus ravelobensis (Zimmermann et al., 1998), Microcebus rufus (Lesson, 1840). These de Doctorat 3ième cycle, University of Antananarivo, Antananarivo.
Rasmussen, DT. 1990. Primate origins – lessons from a neotropical marsupial. American Journal of Primatology 22(4):263–277.Google Scholar
Rasmussen, DT. 2002. The origin of primates. In Hartwig, W (ed.), The Primate Fossil Record (pp. 5–9). Cambridge University Press, Cambridge.
Rasoazanabary, E. 2006. Male and female activity patterns in Microcebus murinus during the dry season at Kirindy Forest, western Madagascar. International Journal of Primatology 27(2):437–464.Google Scholar
Ravosa, MJ, Dagosto, M (eds). 2007. Primate Origins: Adaptations and Evolution. Springer, Chicago.
Rendall, D. 2004. Recognizing kin: mechanisms, media, minds, modules, and muddles. In Chapais, B, Berman, CM (eds.), Kinship and Behavior in Primates (pp. 295–316). Oxford University Press, New York.
Rode, JE, Nekaris, A, Markolf, M, et al. 2013. Social organisation of the northern giant mouse lemur Mirza zaza in Sahamalaza, north western Madagascar, inferred from nest group composition and genetic relatedness. Contributions to Zoology 82(2):71–83.Google Scholar
Scheumann, M, Zimmermann, E. 2008. Sex-specific asymmetries in communication sound perception are not related to hand preference in an early primate. BMC Biology 6(3).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(8):1175–1185.Google Scholar
Schmid, J. 1998. Tree holes used for resting by gray mouse lemurs (Microcebus murinus) in Madagascar: insulation capacities and energetic consequences. International Journal of Primatology 19(5):797–809.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(2):125–132.Google Scholar
Schmitt, D, Lemelin, P. 2002. Origins of primate locomotion: gait mechanics of the woolly opossum. American Journal of Physical Anthropology 118(3):231–238.Google Scholar
Schülke, O, Ostner, J. 2005. Big times for dwarfs: social organization, sexual selection, and cooperation in the Cheirogaleidae. Evolutionary Anthropology 14(5):170–185.Google Scholar
Schülke, O, Ostner, J. 2007. Physiological ecology of cheirogaleid primates: variation in hibernation and torpor. Acta Ethologica 10(1):13–21.Google Scholar
Schwab, D. 2000. A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf myoxinus). American Journal of Primatology 51(1):41–60.Google Scholar
Shultz, S, Opie, C, Atkinson, QD. 2011. Stepwise evolution of stable sociality in primates. Nature 479(7372):219–224.Google Scholar
Siemers, BM, Goerlitz, HR, Robsomanitrandrasana, E, et al. 2007. Sensory basis of food detection in wild Microcebus murinus. International Journal of Primatology 28(2):291–304.Google Scholar
Silcox, MT, Boyer, DM, Bloch, JI, Sargis, EJ. 2007. Revisiting the adaptive origins of primates (again). Journal of Human Evolution 53(3):321–324.Google Scholar
Silk, JB. 2002. Kin selection in primate groups. International Journal of Primatology 23(4):849–875.Google Scholar
Silk, JB. 2007. Social components of fitness in primate groups. Science 317(5843):1347–1351.Google Scholar
Silk, JB. 2009. Nepotistic cooperation in non-human primate groups. Philosophical Transactions of the Royal Society B Biological Sciences 364(1533):3243–3254.Google Scholar
Soligo, C, Martin, RD. 2006. Adaptive origins of primates revisited. Journal of Human Evolution 50(4):414–430.Google Scholar
Soligo, C, Müller, AE. 1999. Nails and claws in primate evolution. Journal of Human Evolution 36(1):97–114.Google Scholar
Springer, MS, Murphy, WJ, Eizirik, E, O'Brien, SJ. 2003. Placental mammal diversification and the Cretaceous–Tertiary boundary. Proceedings of the National Academy of Sciences of the United States of America 100(3):1056–1061.Google Scholar
Steiper, ME, Seiffert, ER. 2012. Evidence for a convergent slowdown in primate molecular rates and its implications for the timing of early primate evolution. Proceedings of the National Academy of Sciences of the United States of America 109(16):6006–6011.Google Scholar
Sterck, EHM, Watts, DP, Schaik, CP van. 1997. The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41:291–309.Google Scholar
Sterling, EJ, Nguyen, N, Fashing, PJ. 2000. Spatial patterning in nocturnal prosimians: a review of methods and relevance to studies of sociality. American Journal of Primatology 51(1):3–19.Google Scholar
Stoen, OG, Bellemain, E, Saebo, S, Swenson, JE. 2005. Kin-related spatial structure in brown bears Ursus arctos. Behavioral Ecology and Sociobiology 59(2):191–197.Google Scholar
Strier, KB. 2007. Primate Behavioral Ecology. Allyn and Bacon, San Francisco.
Sussman, RW. 1991. Primate origins and the evolution of angiosperms. American Journal of Primatology 23(4):209–223.Google Scholar
Sussman, RW, Raven, PH. 1978. Pollination by lemurs and marsupials – archaic coevolutionary system. Science 200(4343):731–736.Google Scholar
Sussman, RW, Rasmussen, DT, Raven, PH. 2013. Rethinking primate origins again. American Journal of Primatology 75(2):95–106.Google Scholar
Tavaré, S, Marshall, CR, Will, O, Soligo, C, Martin, RD. 2002. Using the fossil record to estimate the age of the last common ancestor of extant primates. Nature 416:726–729.Google Scholar
Thorén, S, Quietzsch, F, Schwochow, D, et al. 2011. 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(3):566–586.Google Scholar
Toussaint, S, Reghem, E, Chotard, H, et al. 2013. Food acquisition on arboreal substrates by the grey mouse lemur: implication for primate grasping evolution. Journal of Zoology 291(4):235–242.Google Scholar
Waser, PM, Jones, WT. 1983. Natal philopatry among solitary mammals. Quarterly Review of Biology 58(3):355–390.Google Scholar
Weidt, A, Hagenah, N, Randrianambinina, B, Radespiel, U, Zimmermann, E. 2004. Social organization of the golden brown mouse lemur (Microcebus ravelobensis). American Journal of Physical Anthropology 123(1):40–51.Google Scholar
Whiten, A, Goodall, J, McGrew, WC, et al. 1999. Cultures in chimpanzees. Nature 399(6737):682–685.Google Scholar
Widdig, A. 2007. Paternal kin discrimination: the evidence and likely mechanisms. Biological Review 82(2):319–334.Google Scholar
Widdig, A. 2013. The impact of male reproductive skew on kin structure and sociality in multi-male groups. Evolutionary Anthropology 22(5):239–250.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(1):213–227.Google Scholar
Yurk, H, Barrett-Lennard, L, Ford, JKB, Matkin, CO. 2002. Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Animal Behaviour 63:1103–1119.Google Scholar
Zimmermann, E. 1990. Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships. Zeitschrift Fur Zoologische Systematik Und Evolutionsforschung 28(3):217–239.Google Scholar
Zimmermann, E. 1995a. Acoustic communication in nocturnal prosimians. In Alterman, L, Doyle, GA, Izard, MK (eds.), Creatures of the Dark (pp. 311–330). Plenum Press, New York.
Zimmermann, E. 1995b. Loud calls in nocturnal prosimians: structure, evolution and ontogeny. In Zimmermann, E, Newman, JD, Jurgens, U (eds.), Current Topics in Primate Vocal Communication (pp. 47–72). Plenum Press, New York.
Zimmermann, E. 2010. Vocal expression of emotion in a nocturnal prosimian primate group, mouse lemurs. In Brudzynski, SM (ed.), Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach (pp. 215–225). Academic Press, Oxford.
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

Save book to Kindle

To save this book to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats