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
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
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Bonner JT (1965) Size and cycle. Princeton University Press, USA
Bourlière F, Petter-Rousseaux A (1966) Existence probable d’un rythme metabolique saisonnier chez les Cheirogaleinae (Lemuroidea). Folia Primatol 4:249–256
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
Brotherton PNM, Rhodes A (1996) Monogamy without biparental care in a dwarf antelope. Proc R Soc Lond B 263:23–29
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47
Chesser RK (1991) Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129:573–583
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
Clutton-Brock TH, Harvey PH (1978) Mammals, resources and reproductive strategies. Nature 273:191–195
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
Cowlishaw G, Dunbar R (2000) Primate conservation biology. The University of Chicago Press, Chicago
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
Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate. Nature 429:825–826, 24 June
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
Dunbar RIM (1995) The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim Behav 50:1057–1070
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
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
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
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
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
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
Foerg R (1982) Reproduction in Cheirogaleus medius. Folia Primatol 39(1–2):49–62
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
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
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
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
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
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
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
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
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
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
Hedrick P (2005) Large variance in reproductive success and the N e/N ratio. Evolution 59:1596–1599
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
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
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
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
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
Lewontin RC (1966) On the measurement of relative variability. Syst Zool 15:141–142
Lott DF (1991) Intraspecific variation in the social system of wild vertebrates. Cambridge University Press, Cambridge
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
Manly B (1997) Randomisation, bootstrap and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, London
Moore J (1984) Female transfer in primates. Int J Primatol 5:537–589
Müller AE (1998) A preliminary report on the social organisation of Cheirogaleus medius (Cheirogaleidae; Primates) in North–West Madagascar. Folia Primatol 69:160–166
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
Nei M (1978) Estimation of average of heterozygosity and genetic distance from small number of individuals. Genetics 89:583–590
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
Perret M (1996) Manipulation of sex ratio at birth by urinary cues in a prosimian primate. Behav Ecol Sociobiol 38:259–266
Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127
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
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
Pope T (2000) The evolution of male philopatry in neotropical monkeys. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 219–235
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
Reichard U (1995) Extra-pair copulations in a monogamous gibbon. Ethology 100:99–112
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
Robbins M (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47
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
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Ecol Evol 9(3):552–569
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by coalescent and other methods. Bioinformatics 19:2496–2497
Schradin C, Pillay N (2005) Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107
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
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
Smale L, Nunes S, Holekamp KE (1997) Sexually dimorphic dispersal in mammals: patterns, causes, and consequences. Adv Study Behav 26:181–250
Sommer S (2001) Reproductive ecology of the endangered monogamous Malagasy giant jumping rat, Hypogeomys antimena. Mammal Biol 66:111–115
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
Sugg D, Chesser R (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155
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
Tajima F (1989) Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123:585–595
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
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
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
Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
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
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
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
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
Ziegler TE, Snowdon CT (2000) Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Horm Behav 38:159–167
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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DOI: https://doi.org/10.1007/s00265-006-0323-9