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Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the roles of social setting and female mate choice

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Abstract

Extra-pair paternity (EPP) can be influenced by both social setting and female mate choice. If evidence suggests that females try to obtain extra-pair copulations (EPCs) in order to gain genetic benefits when mated to a homozygous and/or to a related male, females may not be able to choose freely among extra-pair mates (EPMs) as the social mate may constrain female access to EPMs. In this study, we investigated, first, how EPP depended on social setting and specifically on the number of subordinate males in the family group in a highly social and monogamous mammal, the alpine marmot. Second, we investigated how EPP depended on female mate choice for genetic benefits measured as male mate-heterozygosity and within-pair relatedness. Our results reveal, first, that EPP depended on the social setting, increasing with the number of subordinate males. Second, EPPs were related to relatedness between mates. Third, EPMs were found to be more heterozygous than within-pair males. Thus, social setting may constrain female choice by limiting opportunities for EPC. However, after accounting for social confounding factors, female choice for genetic benefits may be a mechanism driving EPP in monogamous species.

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References

  • Allainé D (2000) Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behav Processes 51:21–34

    Article  PubMed  Google Scholar 

  • Allainé D, Brondex F, Graziani L, Coulon J, Till Bottraud I (2000) Male-biased sex ratio in litters of alpine marmots supports the helper repayment hypothesis. Behav Ecol 11:507–514

    Article  Google Scholar 

  • Allainé D, Theuriau F (2004) Is there an optimal number of helpers in alpine marmot family groups? Behav Ecol 15:914–924

    Google Scholar 

  • Arnold W (1990a) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237

    Google Scholar 

  • Arnold W (1990b) The evolution of marmot sociality: II. Costs and benefits of joint hibernation. Behav Ecol Sociobiol 27:239–246

    Google Scholar 

  • Arnold W (1993) Social evolution in marmots and the adaptive value of joint hibernation. Verh Dtsch Zool Ges 86:79–93

    Google Scholar 

  • Arnold W, Dittami J (1997) Reproductive suppression in male alpine marmots. Anim Behav 53:53–66

    Article  Google Scholar 

  • Arnold W, Klinkitch M, Tautz D (1994) Molecular analysis of the mating system of alpine marmots (Marmota marmota). Verh Dtsch Zool Ges 87:27

    Google Scholar 

  • Bel MC, Coulon J, Sreng L, Allainé D, Bagneres AG, Clement JL (1999) Social signals involved in scent-marking behavior by cheek-rubbing in alpine marmots (Marmota marmota). J Chem Ecol 25:2267–2283

    Article  CAS  Google Scholar 

  • Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614

    Article  Google Scholar 

  • Birkhead TR, Atkin L, Møller AP (1987) Copulation behaviour of birds. Behaviour 101:101–133

    Google Scholar 

  • Blouin SF, Blouin M (1988) Inbreeding avoidance behaviors. Trends Ecol Evol 29:1–7

    Google Scholar 

  • Brotherton PNM, Pemberton JM, Komers PE, Malarky G (1997) Genetic and behavioural evidence of monogamy in a mammal, Kirk's dik-dik (Madoqua kirkii). Proc R Soc Lond B 264:675–681

    Article  CAS  Google Scholar 

  • Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65

    Article  Google Scholar 

  • Calf K, Downs C, Cherry M (2003) Territoriality and breeding success in the Cape Sugarbird (Promerops cafer). Emu 103:29–35

    Article  Google Scholar 

  • Carlin JB, Wolfe R, Brown CH, Gelman A (2001) A case study on the choice, interpretation and checking of multilevel models for longitudinal binary outcomes. Biostatistics 2:397–416

    Article  PubMed  CAS  Google Scholar 

  • Carter CS, Getz LL, Cohen-Parsons M (1986) Relationships between social organisation and behavioural endocrinology in a monogamous mammal. Adv Study Behav 16: 109–145

    Article  Google Scholar 

  • Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living island population. Evolution 53:1259–1267

    Article  Google Scholar 

  • Coulon J, Graziani L, Allainé D, Bel MC, Pouderoux S (1995) Infanticide in the alpine marmot (Marmota marmota). Ethol Ecol Evol 7:191–194

    Article  Google Scholar 

  • Coulson TN, Pemberton JM, Albon SD, Beaumont M, Marshall TC, Slate J, Guinness FE, Clutton-Brock TH (1998) Microsatellites reveal heterosis in red deer. Proc R Soc Lond B 265:489–495

    Article  CAS  Google Scholar 

  • Da Silva A, Luikart G, Yoccoz NG, Cohas A, Allainé A (2005) Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota). Cons Gen in press

  • Da Silva A, Luikart G, Allainé D, Gautier P, Taberlet P, Pompanon F (2003) Isolation and characterization of microsatellites in European alpine marmots (Marmota marmota). Mol Ecol Notes 3:189–190

    Article  CAS  Google Scholar 

  • Diggle PJ, Heagerty PJ, Liang KY, Zeger SL (2002) Analysis of longitudinal data, 2nd edn. Oxford University Press, Oxford

  • Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, Van Den Bussche RA (2001) Major-histocompatibility-complex associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution 55:616–625

    Article  PubMed  CAS  Google Scholar 

  • Double MC, Cockburn A (2003) Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proc R Soc Lond B 270:379–384

    Article  Google Scholar 

  • Emlen ST (1982) The evolution of helping: II. The role of behavioural conflict. Am Nat 119: 40–53

    Article  Google Scholar 

  • Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU (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 

  • Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    Article  PubMed  CAS  Google Scholar 

  • Foltz DW (1981) Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionatus. Am Nat 117:665–675

    Article  Google Scholar 

  • Frey-Roos F (1998) Geschlechtsspezifisches Abwanderungsmuster beim Alpenmurmeltier (Marmota marmota). Ph.D. thesis, Philipps University, Germany

  • Girman DJ, Mills MGL, Geffen E, Wayne RK (1997) A molecular genetic analysis of social structure, dispersal and interpack relationships of 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 (1998a) Extra-pair paternity in the monogamous alpine marmot revealed by nuclear DNA microsatellite analysis. Behav Ecol Sociobiol 43:281–288

    Article  Google Scholar 

  • Goossens B, Waits LP, Taberlet P (1998b) Plucked hair samples as a source of DNA: reliability of dinucleotide microsatellite genotyping. Mol Ecol 7:1237–1241

    Article  PubMed  CAS  Google Scholar 

  • Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds. Oxford University Press, Oxford, pp 21–52

    Google Scholar 

  • Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Grimm V, Dorndorf N, Frey Roos F, Wissel C, Wyszomirski T, Arnold W (2003) Modelling the role of social behavior in the persistence of the alpine marmot Marmota marmota. Oikos 102:124–136

    Article  Google Scholar 

  • Hacklander K, Arnold W (1999) Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota). Behav Ecol 10: 592–597

    Article  Google Scholar 

  • Hacklander K, Mostl E, Arnold W (2003) Reproductive suppression in female alpine marmots, Marmota marmota. Anim Behav 65:1133–1140

    Article  Google Scholar 

  • Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol Ecol 9:2163–2165

    Article  PubMed  CAS  Google Scholar 

  • Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474

    Article  PubMed  Google Scholar 

  • Heller KG, Achmann R, Witt K (1993) Monogamy in the bat Rhinolophus sedulus? Z Saugetierkd 58:376–377

    Google Scholar 

  • Hoi Leitner M, Hoi H, Romero-Pujante M, Valera F (1999) Female extra-pair behaviour and environmental quality in the serin (Serinus serinus): a test of the ‘constrained female hypothesis’. Proc R Soc Lond B 266:1021–1026

    Article  Google Scholar 

  • Horton NJ, Lipsitz SR (1999) Review of software to fit generalized estimating equation regression models. Am Stat 53:160–169

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  PubMed  CAS  Google Scholar 

  • Johnsen A, Lifjeld JT, Rohde PA, Primmer CR, Ellegren H (1998) Sexual conflict over fertilizations: female bluethroats escape male paternity guards. Behav Ecol Sociobiol 43:401–408

    Article  Google Scholar 

  • Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

  • Klinkitch M (1993) Untersuchugen zum paarungssystem des Alpenmurmeltiers, Marmota M. marmota mittels DNA fingerprinting. Ph.D. thesis, University of Munich, Germany

  • Kokko H, Johnstone R (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B 266:571–578

    Article  Google Scholar 

  • Komdeur J (2001) Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proc R Soc Lond B 268:2103–2111

    Article  CAS  Google Scholar 

  • Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22

    Article  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    PubMed  CAS  Google Scholar 

  • Magnolon S (1999) Dispersion natale chez la marmotte alpine (Marmota marmota): modalités et effet de quelques facteurs proximaux. Ph.D. thesis, Université de Tours

  • Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim Conserv 3:241–248

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB and Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Matsubara M (2003) Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int J Primatol 24:1057–1075

    Article  Google Scholar 

  • Perrin C, Allainé D, Le Berre M (1993) Socio-spatial organization and activity distribution of the alpine marmot Marmota marmota: preliminary results. Ethology 93:21–30

    Article  Google Scholar 

  • Peters A, Astheimer L, Cockburn A (2001) The annual testosterone profile in cooperatively breeding superb fairy-wrens, Malurus cyaneus, reflects their extreme infidelity. Behav Ecol Sociobiol 50:519–527

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, Berlin Heidelberg New York

  • Plaistow SJ, Bollache L, Cezilly F (2003) Energetically costly precopulatory mate guarding in the amphipod Gammarus pulex: causes and consequences. Anim Behav 65:683–691

    Article  Google Scholar 

  • Price MV, Waser NM (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature 277:294–297

    Article  Google Scholar 

  • Queller D, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43: 258–275

    Article  Google Scholar 

  • R Development Core Team (2003) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Ralls K, Harvey PH, Lyles AM (1986) Inbreeding in natural populations of birds and mammals. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, MA, pp 35–56

    Google Scholar 

  • Rassmann K, Arnold W, Tautz D (1994) Low genetic variability in a natural alpine marmot population (Marmota marmota, Sciuridae) revealed by DNA fingerprinting. Mol Ecol 3:347–353

    PubMed  CAS  Google Scholar 

  • Rätti O, Hovi M, Lundberg A, Tegelström H, Alatalo RV (1995) Extra-paternity and male characteristics in the pied flycatcher. Behav Ecol Sociobiol 37:419–425

    Article  Google Scholar 

  • Raymond M, Rousset R (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Reeve HK, Emlen ST (2000) Reproductive skew and group size: an N-person staying incentive model. Behav Ecol 11:640–647

    Article  Google Scholar 

  • Ribble DO (1991) The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166

    Article  Google Scholar 

  • Richardson PRK (1987) Aardwolf mating system: overt cuckoldry in an apparently monogamous mammal. S Afr J Sci 83:405–410

    Google Scholar 

  • Richardson DS, Burke T (2001) Extrapair paternity and variance in reproductive success related to breeding density in Bullock's orioles. Anim Behav 62:519–525

    Article  Google Scholar 

  • Richardson DS, Jury F, Blaakmeer K, Komdeur J, Burke T (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10:2263–2273

    Article  PubMed  CAS  Google Scholar 

  • Shellman Reeve JS, Reeve HK (2000) Extra-pair paternity as the result of reproductive transactions between paired mates. Proc R Soc Lond B 267:2543–2546

    Article  CAS  Google Scholar 

  • Shields WM (1983) Optimal inbreeding and the evolution of phylopatry. In: Swingland IR Greenwood PJ (eds) The ecology of animal movement. Clarendon, Oxford, pp 132–159

    Google Scholar 

  • Sillero-Zubiri C, Gottelli D, Macdonald DW (1996) Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav Ecol Sociobiol 38:331–340

    Article  Google Scholar 

  • Slagsvold T, Dale S (1994) Why do female pied flycatchers mate with already mated males: deception or restricted mate sampling? Behav Ecol Sociobiol 34:239–235

    Article  Google Scholar 

  • Slate J, Marshall TC and Pemberton JM (2000a) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808

    Article  PubMed  CAS  Google Scholar 

  • Slate J, Kruuk LEB, Marshall TC, Pemberton JM, Clutton-Brock TH (2000b) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc Lond B 267:1657–1662

    Article  CAS  Google Scholar 

  • Sommer S, Tichy H (1999) Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antimena, the endangered, largest endemic Malagasy rodent. Mol Ecol 8:1259–1272

    Article  PubMed  CAS  Google Scholar 

  • Verhencamp SL (1983) Optimal degree of skew in reproductive societies. Am Zool 23:327–335

    Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates and conflict. Ann Rev Ecol Syst 34:365–396

    Article  Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

  • Wolff JO (1992) Parents suppress reproduction and stimulate dispersal in opposite-sex juvenile white-footed mice. Nature 359: 409–410

    Article  PubMed  CAS  Google Scholar 

  • Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134

    Article  PubMed  Google Scholar 

  • Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42:121–130

    Article  PubMed  CAS  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry: I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717

    Article  Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063

    Article  Google Scholar 

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Acknowledgements

We thank all students involved in the trapping of alpine marmots at La Sassière. We would also like to thank Joanna Setchell and Jos Milner for editing the English. We are grateful to Dan Blumstein and David Westneat for their constructive comments on earlier version of the manuscript. Thanks are finally extended to authorities of the Vanoise National Park for granting us permission to work in La Grande Sassière Nature Reserve. Financial support was received from CNRS (France) and the Région Rhônes-Alpes (XI plan Etat-Région). The experiments conducted comply with current French laws.

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Correspondence to A. Cohas.

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Communicated by E. Korpimäki

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Cohas, A., Yoccoz, N.G., Da Silva, A. et al. 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 (2006). https://doi.org/10.1007/s00265-005-0086-8

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