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Genetic structure, lack of sex-biased dispersal and behavioral flexibility in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius

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Abstract

Mating system and dispersal patterns influence the spatio-genetic structure within and between populations. Among mammals, monogamy is rare, and its socio-genetic consequences have not been studied in detail before. The goal of our study was to investigate population history, demographic structure, and dispersal patterns in a population of pair-living fat-tailed dwarf lemurs, Cheirogaleus medius, a small, nocturnal primate from western Madagascar, and to infer their underlying behavioral mechanisms. Tissue samples for DNA extraction were obtained from a total of 140 individuals that were captured in two subpopulations about 3 km apart. Analyses of mtDNA variability at the population level revealed very low levels of genetic variability combined with high haplotype diversity, which is indicative of a recent population bottleneck. We found no evidence for spatial clustering of same-sexed individuals with identical haplotypes within each of two subpopulations but significant clustering between them. Thus, a high level of local subpopulation differentiation was observed (F ST = 0.230). The sexes showed equal variances in the number of individuals representing each haplotype, as well as equal levels of aggregation of identical haplotypes. Hence, both sexes disperse from their natal area, one pattern expected in a pair-living mammal. There is a possibility of behavioral and social flexibility in this species, however, because we documented pronounced differences in density and sex ratio between the two subpopulations, suggesting that single study sites or populations may not be representative of a given local population or even species.

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References

  • Altmann J (1990) Primate males go where the females are. Anim Behav 39:193–195

    Article  Google Scholar 

  • Alves MJ, Coelho H, Collares-Pereira MJ, Coelho MM (2001) Mitochondrial DNA variation in the highly endangered cyprinid fish Anaecypris hispanica: importance for conservation. Heredity 87:463–473

    Article  PubMed  CAS  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Bonner JT (1965) Size and cycle. Princeton University Press, USA

    Google Scholar 

  • Bourlière F, Petter-Rousseaux A (1966) Existence probable d’un rythme metabolique saisonnier chez les Cheirogaleinae (Lemuroidea). Folia Primatol 4:249–256

    PubMed  Google Scholar 

  • Brotherton PNM, Komers PE (2003) Mate guarding and the evolution of social monogamy in mammals. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 42–58

    Google Scholar 

  • Brotherton PNM, Rhodes A (1996) Monogamy without biparental care in a dwarf antelope. Proc R Soc Lond B 263:23–29

    Article  CAS  Google Scholar 

  • Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  • Chesser RK (1991) Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129:573–583

    PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Google Scholar 

  • Clutton-Brock TH, Harvey PH (1978) Mammals, resources and reproductive strategies. Nature 273:191–195

    Article  PubMed  CAS  Google Scholar 

  • Cohas A, Yoccoz NG, Da Silva A, Goossens B, Allainé D (2006) Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the roles of social setting and female mate choice. Behav Ecol Sociobiol 59:597–605

    Article  Google Scholar 

  • Cowlishaw G, Dunbar R (2000) Primate conservation biology. The University of Chicago Press, Chicago

    Google Scholar 

  • Dausmann KH, Ganzhorn JU, Heldmaier G (2000) Body temperature and metabolic rate of a hibernating primate in Madagascar: preliminary results from a field. In: Heldmaier G, Klingenspor M (eds), Life in cold. Springer, Berlin, pp. 41–48

    Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate. Nature 429:825–826, 24 June

    Article  PubMed  CAS  Google Scholar 

  • Degen B, Petit R, Kremer A (2001) SGS—Spatial Genetic Software: a computer program for analysis of spatial genetic and phenotypic structures of individuals and populations. J Heredity 92:447–449

    Article  CAS  Google Scholar 

  • Dunbar RIM (1995) The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim Behav 50:1057–1070

    Article  Google Scholar 

  • Faulkes CG, Arruda MF, Monteiro da Cruz MAO (2003) Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Mol Ecol 12:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellites patterns. Proc R Soc Lond B 264:127–132

    Article  CAS  Google Scholar 

  • Fernando P, Lande R (2000) Molecular genetic and behavioural analysis of social organization in the Asian elephant (Elephas maximus). Behav Ecol Sociobiol 48:84–91

    Article  Google Scholar 

  • Fietz J (1999) Monogamy as a rule rather than exception in nocturnal lemurs: the case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethology 105:259–272

    Article  Google Scholar 

  • Fietz J, Dausmann K (2003) Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol 74(5–6):246–58

    Article  PubMed  Google Scholar 

  • Fietz J, Zischler H, Schwiegk C (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17

    Article  Google Scholar 

  • Foerg R (1982) Reproduction in Cheirogaleus medius. Folia Primatol 39(1–2):49–62

    Article  PubMed  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Use of molecular genetics in forensics and to understand species biology. In: Introduction to conservation genetics. Cambridge University Press, Cambridge, pp 471–501

    Google Scholar 

  • Fredsted T, Pertoldi C, Olesen JM, Eberle M, Kappeler P (2004) Microgeographic heterogeneity in spatial distribution and mtDNA variability of gray mouse lemurs (Microcebus murinus, Primates: Cheirogaleidae). Behav Ecol Sociobiol 56:393–403

    Article  Google Scholar 

  • Fredsted T, Pertoldi C, Schierup MH, Kappeler P (2005) Microsatellite analyses reveal fine-scale genetic structure in grey mouse lemurs (Microcebus murinus). Mol Ecol 14:2363–2373

    Article  PubMed  CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (1999) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of bonobos (Pan panicus) determined from DNA analysis of faecal samples. Proc R Soc Lond B 266:1189–1195

    Article  CAS  Google Scholar 

  • Girman D, Mills M, Geffen E, Wayne R (1997) A molecular genetic analysis of social structure, dispersal, and interpack relationships on the African wild dog (Lycaon pictus). Behav Ecol Sociobiol 40:187–198

    Article  Google Scholar 

  • Goossens B, Graziani L, Waits LP, Farand E, Magnolon S, Coulon J, Bel MC, Taberlet P, Allainé D (1998) Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behav Ecol Sociobiol 43:281–288

    Article  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Hall TA (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hartl DL, Clark AG (1989) Random genetic drift: effective population size. In: principles of population genetics, 2nd edn. Sinauer Associates, Sunderland, MA, pp 61–95

    Google Scholar 

  • Hedrick P (2005) Large variance in reproductive success and the N e/N ratio. Evolution 59:1596–1599

    Article  PubMed  Google Scholar 

  • Hein J, Schierup MH, Wiuf C (2005) Extensions to the basic coalescent. In: Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford University Press, Oxford, pp 104–106

  • Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151

    Article  PubMed  CAS  Google Scholar 

  • Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740

    Article  Google Scholar 

  • Kappeler PM, Wimmer B, Zinner D, Tautz D (2002) The hidden matrilineal group structure of a solitary lemur: implications for primate social evolution. Proc R Soc Lond B 269:1755–1763

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lehman N, Clarkson P, Mech LD, Meier TJ, Wayne RK (1992) A study of genetic relationships within and among wolfpacks using DNA fingerprinting and mitochondrial DNA. Behav Ecol Sociobiol 30:83–94

    Article  Google Scholar 

  • Lewontin RC (1966) On the measurement of relative variability. Syst Zool 15:141–142

    Article  Google Scholar 

  • Lott DF (1991) Intraspecific variation in the social system of wild vertebrates. Cambridge University Press, Cambridge

    Google Scholar 

  • Lukas D, Reynolds V, Boesch C, Vigilant L (2005) To what extent does living in a group mean living with kin? Mol Ecol 14:2181–2196

    Article  PubMed  CAS  Google Scholar 

  • Manly B (1997) Randomisation, bootstrap and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, London

    Google Scholar 

  • Moore J (1984) Female transfer in primates. Int J Primatol 5:537–589

    Google Scholar 

  • Müller AE (1998) A preliminary report on the social organisation of Cheirogaleus medius (Cheirogaleidae; Primates) in North–West Madagascar. Folia Primatol 69:160–166

    Article  Google Scholar 

  • Müller AE, Thalmann U (2002) Biology of the fat-tailed dwarf lemur (Cheirogaleus medius E. Geoffroy 1812): new results from the field. Evol Anthropol (suppl 1):79–82

    Article  Google Scholar 

  • Nei M (1978) Estimation of average of heterozygosity and genetic distance from small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum SM, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 123–166

    Google Scholar 

  • Perret M (1996) Manipulation of sex ratio at birth by urinary cues in a prosimian primate. Behav Ecol Sociobiol 38:259–266

    Article  Google Scholar 

  • Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127

    Article  PubMed  Google Scholar 

  • Petrie M, Doums C, Møller AP (1998) The degree of extra-pair paternity increases with genetic variability. Proc Natl Acad Sci USA 95:9390–9395

    Article  PubMed  CAS  Google Scholar 

  • Petter JJ (1988) Contribution a l’étude du Cheirogaleus medius dans la forêt de Morondava. In: Rakotovao L, Barre V, Sayer J (eds) L’Equilibre des Ecosystemes Forestièrs a Madagascar: Actes d’un Séminaire International. Page Bros, Cambridge, pp 57–60

    Google Scholar 

  • Pope T (2000) The evolution of male philopatry in neotropical monkeys. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 219–235

    Google Scholar 

  • Pusey AE (1992) The primate perspective on dispersal. In: Stenseth NC, Lidicker WZJ (eds) Dispersal: small mammals as a model. Chapman and Hall, London, pp 243–259

    Google Scholar 

  • Reichard U (1995) Extra-pair copulations in a monogamous gibbon. Ethology 100:99–112

    Article  Google Scholar 

  • Reichard U (2003) Monogamy: past and present. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 3–25

    Google Scholar 

  • Robbins M (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47

    Google Scholar 

  • Roberts RL, Williams JR, Wanf AK, Carter CS (1998). Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation. Anim Behav 55:1131–1140

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Ecol Evol 9(3):552–569

    CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Schradin C, Pillay N (2005) Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107

    Article  Google Scholar 

  • Schülke O, Kappeler PM, Zischler H (2004) Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer. Behav Ecol Sociobiol 55:296–310

    Google Scholar 

  • Schulte-Hostedde A, Millar J (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav Ecol Sociobiol 55:272–277

    Article  Google Scholar 

  • Smale L, Nunes S, Holekamp KE (1997) Sexually dimorphic dispersal in mammals: patterns, causes, and consequences. Adv Study Behav 26:181–250

    Article  Google Scholar 

  • Sommer S (2001) Reproductive ecology of the endangered monogamous Malagasy giant jumping rat, Hypogeomys antimena. Mammal Biol 66:111–115

    Google Scholar 

  • Steenbeek R, Sterck E, de Vries H, van Hooff J (2000) Costs and benefits of the one-male, age-graded and all-male phases in wild Thomas’s langur groups. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 130–145

    Google Scholar 

  • Sugg D, Chesser R (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155

    PubMed  CAS  Google Scholar 

  • Surridge A, Bell D, Ibrahim K, Hewitt G (1999) Population structure and genetic variation of European wild rabbits (Oryctolagus cuniculus) in East Anglia. Heredity 82:479–487

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Travis S, Slobodchikoff C, Keim P (1995) Ecological and demographic effects on intraspecific variation in the social system of prairie dogs. Ecology 76:1794–1803

    Article  Google Scholar 

  • Trizio I, Crestaneelo B, Galbusera P, Wayters LA, Matthysen E, Hauffe HC (2005) Geographical distance and physical barriers shape the genetic structure of Eurasian red squirrels (Sciurus vulgaris) in the Italian Alps. Mol Ecol 14:469–81

    Article  PubMed  CAS  Google Scholar 

  • van Schaik CP, Kappeler PM (2003) The evolution of social monogamy in primates. In: Reichard U, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, Cambridge, pp 59–80

    Google Scholar 

  • Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wimmer B, Tautz D, Kappeler P (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol 52:166–175

    Article  Google Scholar 

  • Wise CA, Sraml M, Rubinsztein DC, Easteal S (1997) Comparative nuclear and mitochondrial genome diversity in humans and chimpanzees. Mol Biol Evol 14:707–716

    PubMed  CAS  Google Scholar 

  • Yamagiwa J, Hill DA (1998) Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. Primates 39:257–273

    Google Scholar 

  • Yu N, Jensen-Seaman MI, Chemnick L, Kidd JR, Deinard AS, Ryder O, Kidd KK, Li WH (2003) Low nucleotide diversity in chimpanzees and bonobos. Genetics 164:1511–1518

    PubMed  CAS  Google Scholar 

  • Ziegler TE, Snowdon CT (2000) Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Horm Behav 38:159–167

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We thank Joanna Fietz and Kathrin Daussmann for providing additional genetic samples. We also thank the late Madame Berthe Rakotosamimanana at the Département de Paléontologie et d’Anthropologie Biologique de l’Université d’Antananarivo, the late Albert Randrianjafy and Gilbert Rakotoarisoa of Parc Botanique et Zoologique de Tsimbazaza, Madame Olga Ramilijaona and Daniel Rakotondravony of the Département Biologie Animale de l’Université d’Antananarivo, the members of the Commission Tripartite and the C.A.F.F. of the Direction des Eaux et Forêts, and the CFPF Morondava for their authorization and support of this study. We thank Palle Villesen for programming the permutation test of haplotypes in R. Also, thanks to Stine W. Bjorholm for creating the GIS map and Benoit Goossens for very helpful comments on this manuscript. The German Primate Centre and grants from the WWF Biodiversity Fund and Augustinus Fond, Denmark, financed this work. T. Fredsted was supported by a Ph.D. grant from the Faculty of Science of the University of Aarhus, Denmark.

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Fredsted, T., Schierup, M.H., Groeneveld, L.F. et al. Genetic structure, lack of sex-biased dispersal and behavioral flexibility in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius . Behav Ecol Sociobiol 61, 943–954 (2007). https://doi.org/10.1007/s00265-006-0323-9

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