Modeling the origins of mammalian sociality: moderate evidence for matrilineal signatures in mouse lemur vocalizations

Frontiers in Zoology - Tập 11 - Trang 1-14 - 2014
Sharon E Kessler1,2, Ute Radespiel2, Alida I F Hasiniaina3, Lisette M C Leliveld2,4, Leanne T Nash1, Elke Zimmermann2
1School of Human Evolution and Social Change, Arizona State University, Tempe, USA
2Institute of Zoology, University of Veterinary Medicine Hannover, Hannover, Germany
3Faculté des Sciences, Université de Mahajanga, Mahajanga, Madagascar
4Institute for Behavioural Physiology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany

Tóm tắt

Maternal kin selection is a driving force in the evolution of mammalian social complexity and it requires that kin are distinctive from nonkin. The transition from the ancestral state of asociality to the derived state of complex social groups is thought to have occurred via solitary foraging, in which individuals forage alone, but, unlike the asocial ancestors, maintain dispersed social networks via scent-marks and vocalizations. We hypothesize that matrilineal signatures in vocalizations were an important part of these networks. We used the solitary foraging gray mouse lemur (Microcebus murinus) as a model for ancestral solitary foragers and tested for matrilineal signatures in their calls, thus investigating whether such signatures are already present in solitary foragers and could have facilitated the kin selection thought to have driven the evolution of increased social complexity in mammals. Because agonism can be very costly, selection for matrilineal signatures in agonistic calls should help reduce agonism between unfamiliar matrilineal kin. We conducted this study on a well-studied population of wild mouse lemurs at Ankarafantsika National Park, Madagascar. We determined pairwise relatedness using seven microsatellite loci, matrilineal relatedness by sequencing the mitrochondrial D-loop, and sleeping group associations using radio-telemetry. We recorded agonistic calls during controlled social encounters and conducted a multi-parametric acoustic analysis to determine the spectral and temporal structure of the agonistic calls. We measured 10 calls for each of 16 females from six different matrilineal kin groups. Calls were assigned to their matriline at a rate significantly higher than chance (pDFA: correct = 47.1%, chance = 26.7%, p = 0.03). There was a statistical trend for a negative correlation between acoustic distance and relatedness (Mantel Test: g = -1.61, Z = 4.61, r = -0.13, p = 0.058). Mouse lemur agonistic calls are moderately distinctive by matriline. Because sleeping groups consisted of close maternal kin, both genetics and social learning may have generated these acoustic signatures. As mouse lemurs are models for solitary foragers, we recommend further studies testing whether the lemurs use these calls to recognize kin. This would enable further modeling of how kin recognition in ancestral species could have shaped the evolution of complex sociality.

Tài liệu tham khảo

Hamilton WD: The genetical evolution of social behavior. I and II. J Theor Biol. 1964, 7: 1-52. 10.1016/0022-5193(64)90038-4. Rendall D: Recognizing kin: mechanisms, media, minds, modules, and muddles. Kinship and Behavior in Primates. Edited by: Chapais B, Berman CM. 2004, New York: Oxford University Press, 295-316. Kinship and Behavior in Primates. Edited by: Chapais B, Berman CM. 2004, New York: Oxford University Press Animal Social Complexity: Intelligence, Culture, and Individualized Societies. Edited by: de Waal F, Tyack PL. 2003, Cambridge: Harvard University Press The Evolution of Emotional Communication: From Sounds in Nonhuman Mammals to Speech and Music in Man. 2013. Edited by: Altenmüller E, Schmidt S, Zimmermann E. 2013, Oxford: Oxford University Press Müller AE, Thalmann U: Origin and evolution of primate social organisation: a reconstruction. Biol Rev. 2000, 75: 405-435. 10.1017/S0006323100005533. Shultz S, Opie C, Atkinson QD: Stepwise evolution of stable sociality in primates. Nature. 2011, 479: 219-224. 10.1038/nature10601. Briefer EF, McElligott AG: Social effects on vocal ontogeny in an ungulate, the goat, Capra hircus. Anim Behav. 2012, 83: 991-1000. 10.1016/j.anbehav.2012.01.020. Briefer EF, de la Torre MP, McElligott AG: Mother goats do not forget their kids' calls. P Roy Soc B-Biol Sci. 2012, 279: 3749-3755. 10.1098/rspb.2012.0986. Townsend SW, Hollen LI, Manser MB: Meerkat close calls encode group-specific signatures, but receivers fail to discriminate. Anim Behav. 2010, 80: 133-138. 10.1016/j.anbehav.2010.04.010. Blumstein DT, Nguyen KT, Martin JGA: Ontogenetic variation of heritability and maternal effects in yellow-bellied marmot alarm calls. P Roy Soc B-Biol Sci. 2013, 280: 7- Tyack PL: Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. J Comp Psychol. 2008, 122: 319-331. Yurk H, Barrett-Lennard L, Ford JKB, Matkin CO: Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Anim Behav. 2002, 63: 1103-1119. 10.1006/anbe.2002.3012. Whitehead H, Dillon M, Dufault S, Weilgart L, Wright J: Non-geographically based population structure of south Pacific sperm whales: dialects, fluke-markings and genetics. J Anim Ecol. 1998, 67: 253-262. 10.1046/j.1365-2656.1998.00187.x. Gillam EH, Chaverri G: Strong individual signatures and weaker group signatures in contact calls of Spix's disc-winged bat, Thyroptera tricolor. Anim Behav. 2012, 83: 269-276. 10.1016/j.anbehav.2011.11.002. Chaverri G, Kunz TH: All-offspring natal philopatry in a Neotropical bat. Anim Behav. 2011, 82: 1127-1133. 10.1016/j.anbehav.2011.08.007. Scherrer JA, Wilkinson GS: Evening bat isolation calls provide evidence for heritable signatures. Anim Behav. 1993, 46: 847-860. 10.1006/anbe.1993.1270. Hoffmann F, Musolf K, Penn DJ: Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiol Behav. 2012, 105: 766-771. 10.1016/j.physbeh.2011.10.011. Latham N, Mason G: From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Anim Behav Sci. 2004, 86: 261-289. 10.1016/j.applanim.2004.02.006. Charlton BD, Zhang ZH, Snyder RJ: Vocal cues to identity and relatedness in giant pandas (Ailuropoda melanoleuca). J Acoust Soc Am. 2009, 126: 2721-2732. 10.1121/1.3224720. Rendall D, Notman H, Owren MJ: Asymmetries in the individual distinctiveness and maternal recognition of infant contact calls and distress screams in baboons. J Acoust Soc Am. 2009, 125: 1792-1805. 10.1121/1.3068453. Rendall D, Cheney DL, Seyfarth RM: Proximate factors mediating "contact" calls in adult female baboons (Papio cynocephalus ursinus) and their infants. J Comp Psychol. 2000, 114: 36-46. Rendall D, Rodman PS, Emond RE: Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav. 1996, 51: 1007-1015. 10.1006/anbe.1996.0103. Nunn CL: Maternal recognition of infant calls in ring-tailed lemurs. Folia Primatol (Basel). 2000, 71: 142-146. 10.1159/000021742. Insley SJ, Phillips AV, Charrier I: A review of social recognition in pinnipeds. Aquat Mamm. 2003, 29: 181-201. 10.1578/016754203101024149. McComb K, Moss C, Sayialel S, Baker L: Unusually extensive networks of vocal recognition in African elephants. Anim Behav. 2000, 59: 1103-1109. 10.1006/anbe.2000.1406. Sayigh LS, Tyack PL, Wells RS, Solow AR, Scott MD, Irvine AB: Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Anim Behav. 1998, 57: 41-50. Kessler SE, Scheumann M, Nash LT, Zimmermann E: Paternal kin recognition in the high frequency / ultrasonic range in a solitary foraging mammal. BMC Ecol. 2012, 12: 26-10.1186/1472-6785-12-26. Nash LT: Kinship and behavior among nongregarious nocturnal prosimians: What do we really know?. Kinship and Behavior in Primates. Edited by: Chapais B, Berman CM. 2004, New Yor: Oxford University Press, 200-222. Cartmill M: New views on primate origins. Evol Anthropol. 1992, 1: 105-111. Cartmill M: Rethinking primate origins. Science. 1974, 184: 436-443. 10.1126/science.184.4135.436. Cartmill M: Arboreal adaptations and the origin of the order Primates. The functional and evolutionary biology of primates. Edited by: Tuttle RH. 1972, Chicago: Aldine-Atherton, 97-122. Gebo DL: A shrew-sized origin for primates. Yearb Phys Anthropol. 2004, 47: 40-62. Yearbook of Physical Anthropology] Sussman RW: Primate origins and the evolution of angiosperms. Am J Primatol. 1991, 23: 209-223. 10.1002/ajp.1350230402. Rasmussen DT: Primate origins - Lessons from a neotropical marsupial. Am J Primatol. 1990, 22: 263-277. 10.1002/ajp.1350220406. Rasmussen DT: The origin of primates. The Primate Fossil Record. Edited by: Hartwig W. 2002, Cambridge: Cambridge University Press, 5-9. Martin RD, Soligo C, Tavare S: Primate origins: Implications of a cretaceous ancestry. Folia Primatol (Basel). 2007, 78: 277-296. 10.1159/000105145. Charles-Dominique P, Martin RD: Evolution of lorises and lemurs. Nature. 1970, 227: 257-10.1038/227257a0. Piep M, Radespiel U, Zimmermann E, Schmidt S, Siemers BM: The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus. Anim Behav. 2008, 75: 871-878. 10.1016/j.anbehav.2007.07.008. Radespiel U: Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp. Lemurs: Ecology and Adaptation. Edited by: Gould L, Sauther ML. 2006, New York: Springer, 211-234. Primate Origins: Adaptations and Evolution. Edited by: Ravosa MJ, Dagosto M. 2007, Chicago: Springer Radespiel U, Sarikaya Z, Zimmermann E, Bruford MW: Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus). Behav Ecol Sociobiol. 2001, 50: 493-502. 10.1007/s002650100402. Radespiel U: Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol. 2000, 51: 21-40. Radespiel U, Cepok S, Zietemann V, Zimmermann E: Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. Am J Primatol. 1998, 46: 77-84. 10.1002/(SICI)1098-2345(1998)46:1<77::AID-AJP6>3.0.CO;2-S. Kappeler PM: Nests, tree holes, and the evolution of primate life histories. Am J Primatol. 1998, 46: 7-33. 10.1002/(SICI)1098-2345(1998)46:1<7::AID-AJP3>3.0.CO;2-#. Kappeler PM: Determinants of primate social organization: Comparative evidence and new insights from Malagasy lemurs. Biol Rev Camb Philos Soc. 1997, 72: 111-151. 10.1017/S0006323196004999. Radespiel L, Lutermann H, Schmelting B, Bruford MW, Zimmermann E: Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Anim Behav. 2003, 65: 709-719. 10.1006/anbe.2003.2121. Schliehe-Diecks S, Eberle M, Kappeler PM: Walk the line-dispersal movements of gray mouse lemurs (Microcebus murinus). Behav Ecol Sociobiol. 2012, 66: 1175-1185. 10.1007/s00265-012-1371-y. Eberle M, Kappeler PM: Mouse lemurs in space and time: a test of the socioecological model. Behav Ecol Sociobiol. 2002, 51: 131-139. 10.1007/s002650100409. Eberle M, Kappeler PM: Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behav Ecol Sociobiol. 2006, 60: 582-588. 10.1007/s00265-006-0203-3. Fitch WT, Hauser MD: Vocal production in nonhuman primates: acoustics, physiology, and function constraints on "honest" advertisement. Am J Primatol. 1995, 37: 191-219. 10.1002/ajp.1350370303. Ey E, Pfefferle D, Fischer J: Do age- and sex-related variations reliably reflect body size in non-human primate vocalizations? A review. Primates. 2007, 48: 253-267. 10.1007/s10329-006-0033-y. Owren MJ, Rendall D: An affect-conditioning model of nonhuman primate vocal signaling. Perspect Ethol. Edited by: Owings DH, Beecher MD, Thompson NS. 1997, New York: Plenum Press, 12: 299-346. 10.1007/978-1-4899-1745-4_10. Braune P, Schmidt S, Zimmermann E: Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.). BMC Biol. 2008, 6: 19-10.1186/1741-7007-6-19. Buesching CD, Heistermann M, Hodges JK, Zimmermann E: Multimodal oestrus advertisement in a small nocturnal prosimian. Microcebus murinus. Folia Primatol (Basel). 1998, 69: 295-308. 10.1159/000052718. Scheumann M, Zimmermann E, Deichsel G: Context-specific calls signal infants' needs in a strepsirrhine primate, the gray mouse lemur (Microcebus murinus). Dev Psychobiol. 2007, 49: 708-718. 10.1002/dev.20234. Zimmermann E: Vocal expression of emotion in a nocturnal prosimian primate group, mouse lemurs. Handbook of Mammalian Vocalizations: An Integrative Neuroscience Approach. Edited by: Brudzynski SM. 2009, Oxford: Academic Press, 215-225. Leliveld LMC, Scheumann M, Zimmermann E: Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus). J Acoust Soc Am. 2011, 129: 2278-2288. 10.1121/1.3559680. Goodnight KF, Queller DC: Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol. 1999, 8: 1231-1234. 10.1046/j.1365-294x.1999.00664.x. Queller DC, Goodnight KF: Estimating relatedness using genetic markers. Evolution. 1989, 43: 258-275. 10.2307/2409206. Rendall D, Kollias S, Ney C, Lloyd P: Pitch (F-0) and formant profiles of human vowels and vowel-like baboon grunts: The role of vocalizer body size and voice-acoustic allometry. J Acoust Soc Am. 2005, 117: 944-955. 10.1121/1.1848011. Zimmermann E: Ontogeny of acoustic communication in prosimian primates. Primatology Today. Edited by: Ehara A, Kimura T, Takenaka O, Iwamoto M. 1991, Amsterdam: Elsevier Science, 337-340. Sharp SP, McGowan A, Wood MJ, Hatchwell BJ: Learned kin recognition cues in a social bird. Nature. 2005, 434: 1127-1130. 10.1038/nature03522. Rendall D, Owren MJ, Rodman PS: The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. J Acoust Soc Am. 1998, 103: 602-614. 10.1121/1.421104. Mitani JC, GrosLouis J, Macedonia JM: Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. Int J Primatol. 1996, 17: 569-583. 10.1007/BF02735192. Eberle M, Kappeler PM: Mutualism, reciprocity, or kin selection? Cooperative rescue of a conspecific from a boa in a nocturnal solitary forager the gray mouse lemur. Am J Primatol. 2008, 70: 410-414. 10.1002/ajp.20496. Hatchwell BJ: Cryptic kin selection: Kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology. 2010, 116: 203-216. 10.1111/j.1439-0310.2009.01732.x. Widdig A: The impact of male reproductive skew on kin structure and sociality in multi-male groups. Evol Anthropol. 2013, 22: 239-250. 10.1002/evan.21366. Grafen A: Do animals really recognize kin?. Anim Behav. 1990, 39: 42-54. 10.1016/S0003-3472(05)80724-9. Tang-Martinez Z: The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation. Behav Process. 2001, 53: 21-40. 10.1016/S0376-6357(00)00148-0. Fripp D, Owen C, Quintana-Rizzo E, Shapiro A, Buckstaff K, Jankowski K, Wells R, Tyack P: Bottlenose dolphin (Tursiops truncatus) calves appear to model their signature whistles on the signature whistles of community members. Anim Cogn. 2005, 8: 17-26. 10.1007/s10071-004-0225-z. Radespiel U, Dal Secco V, Drogemuller C, Braune P, Labes E, Zimmermann E: Sexual selection, multiple mating and paternity in grey mouse lemurs, Microcebus murinus. Anim Behav. 2002, 63: 259-268. 10.1006/anbe.2001.1924. Seutin G, White BN, Boag PT: Preservation of avian blood and tissue samples for DNA analyses. Can J Zool. 1991, 69: 82-90. 10.1139/z91-013. Wrogemann D, Radespiel U, Zimmermann E: Comparison of reproductive characteristics and changes in body weight between captive populations of rufous and gray mouse lemurs. Int J Primatol. 2001, 22: 91-108. 10.1023/A:1026418132281. Radespiel U, Funk SM, Zimmermann E, Bruford MW: Isolation and characterization of microsatellite loci in the grey mouse lemur (Microcebus murinus) and their amplification in the family Cheirogaleidae. Mol Ecol Notes. 2001, 1: 16-18. Hapke A, Eberle M, Zischler H: Isolation of new microsatellite markers and application in four species of mouse lemurs (Microcebus sp.). Mol Ecol Notes. 2003, 3: 205-208. 10.1046/j.1471-8286.2003.00398.x. Wimmer B, Tautz D, Kappeler PM: The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol. 2002, 52: 166-175. 10.1007/s00265-002-0497-8. Radespiel U, Juric M, Zimmermann E: Sociogenetic structures, dispersal and the risk of inbreeding in a small nocturnal lemur, the golden-brown mouse lemur (Microcebus ravelobensis). Behaviour. 2009, 146: 607-628. 10.1163/156853909X426372. Guschanski K, Olivieri G, Funk SM, Radespiel U: MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis. Conserv Genet. 2007, 8: 809-821. 10.1007/s10592-006-9228-4. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121. Goudet J: Fstat version 1.2: A computer program to calculate Fstatistics. J Hered. 1995, 86: 485-486. Harrison HB, Saenz-Agudelo P, Planes S, Jones GP, Berumen ML: Relative accuracy of three common methods of parentage analysis in natural populations. Mol Ecol. 2013, 22: 1158-1170. 10.1111/mec.12138. Csilléry K, Johnson T, Beraldi D, Clutton-Brock T, Coltman D, Hansson B, Spong G, Pemberton JM: Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics. 2006, 173: 2091-2101. 10.1534/genetics.106.057331. Rode JE, Nekaris A, Markolf M, Schliehe-Diecks S, Seiler M, Radespiel U, Schwitzer C: Social organisation of the northern giant mouse lemur Mirza zaza in Sahamalaza, north western Madagascar, inferred from nest group composition and genetic relatedness. Contrib Zool. 2013, 82: 71-83. Van Horn RC, Altmann J, Alberts SC: Can't get there from here: inferring kinship from pairwise genetic relatedness. Anim Behav. 2008, 75: 1173-1180. 10.1016/j.anbehav.2007.08.027. Botstein D, White RL, Skolnick M, Davis RW: Construction of a genetic-linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet. 1980, 32: 314-331. Jamieson A, Taylor SS: Comparisons of three probability formulae for parentage exclusion. Anim Genet. 1997, 28: 397-400. 10.1111/j.1365-2052.1997.00186.x. Eberle M, Kappeler PM: Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol. 2004, 57: 77-90. 10.1007/s00265-004-0826-1. Eberle M, Kappeler PM: Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol. 2004, 57: 91-100. 10.1007/s00265-004-0823-4. Mundry R, Sommer C: Discriminant function analysis with nonindependent data: consequences and an alternative. Anim Behav. 2007, 74: 965-976. 10.1016/j.anbehav.2006.12.028. Liedloff AC: Mantel Nonparametric Test Calculator Version 2.0. School of Natural Resource Sciences. 1999, Australia: Queensland University of Technology