Behavioral Ecology and Sociobiology

, Volume 59, Issue 5, pp 597–605 | Cite as

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

  • A. Cohas
  • N. G. Yoccoz
  • A. Da Silva
  • B. Goossens
  • D. Allainé
Original Paper

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.

Keywords

Constrained-female hypothesis Heterozygosity Mating system Microsatellite Relatedness Inbreeding Good genes 

Notes

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.

References

  1. Allainé D (2000) Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behav Processes 51:21–34PubMedCrossRefGoogle Scholar
  2. 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 11:507–514CrossRefGoogle Scholar
  3. Allainé D, Theuriau F (2004) Is there an optimal number of helpers in alpine marmot family groups? Behav Ecol 15:914–924Google Scholar
  4. Arnold W (1990a) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237Google Scholar
  5. Arnold W (1990b) The evolution of marmot sociality: II. Costs and benefits of joint hibernation. Behav Ecol Sociobiol 27:239–246Google Scholar
  6. Arnold W (1993) Social evolution in marmots and the adaptive value of joint hibernation. Verh Dtsch Zool Ges 86:79–93Google Scholar
  7. Arnold W, Dittami J (1997) Reproductive suppression in male alpine marmots. Anim Behav 53:53–66CrossRefGoogle Scholar
  8. Arnold W, Klinkitch M, Tautz D (1994) Molecular analysis of the mating system of alpine marmots (Marmota marmota). Verh Dtsch Zool Ges 87:27Google Scholar
  9. 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 25:2267–2283CrossRefGoogle Scholar
  10. Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614CrossRefGoogle Scholar
  11. Birkhead TR, Atkin L, Møller AP (1987) Copulation behaviour of birds. Behaviour 101:101–133Google Scholar
  12. Blouin SF, Blouin M (1988) Inbreeding avoidance behaviors. Trends Ecol Evol 29:1–7Google Scholar
  13. 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 264:675–681CrossRefGoogle Scholar
  14. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65CrossRefGoogle Scholar
  15. Calf K, Downs C, Cherry M (2003) Territoriality and breeding success in the Cape Sugarbird (Promerops cafer). Emu 103:29–35CrossRefGoogle Scholar
  16. 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 2:397–416PubMedCrossRefGoogle Scholar
  17. Carter CS, Getz LL, Cohen-Parsons M (1986) Relationships between social organisation and behavioural endocrinology in a monogamous mammal. Adv Study Behav 16: 109–145CrossRefGoogle Scholar
  18. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living island population. Evolution 53:1259–1267CrossRefGoogle Scholar
  19. Coulon J, Graziani L, Allainé D, Bel MC, Pouderoux S (1995) Infanticide in the alpine marmot (Marmota marmota). Ethol Ecol Evol 7:191–194CrossRefGoogle Scholar
  20. 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 265:489–495CrossRefGoogle Scholar
  21. 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 Google Scholar
  22. 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 3:189–190CrossRefGoogle Scholar
  23. Diggle PJ, Heagerty PJ, Liang KY, Zeger SL (2002) Analysis of longitudinal data, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  24. 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 55:616–625PubMedCrossRefGoogle Scholar
  25. Double MC, Cockburn A (2003) Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proc R Soc Lond B 270:379–384CrossRefGoogle Scholar
  26. Emlen ST (1982) The evolution of helping: II. The role of behavioural conflict. Am Nat 119: 40–53CrossRefGoogle Scholar
  27. 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 49:8–17CrossRefGoogle Scholar
  28. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717PubMedCrossRefGoogle Scholar
  29. Foltz DW (1981) Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionatus. Am Nat 117:665–675CrossRefGoogle Scholar
  30. Frey-Roos F (1998) Geschlechtsspezifisches Abwanderungsmuster beim Alpenmurmeltier (Marmota marmota). Ph.D. thesis, Philipps University, GermanyGoogle Scholar
  31. 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 40:187–198CrossRefGoogle Scholar
  32. 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 43:281–288CrossRefGoogle Scholar
  33. Goossens B, Waits LP, Taberlet P (1998b) Plucked hair samples as a source of DNA: reliability of dinucleotide microsatellite genotyping. Mol Ecol 7:1237–1241PubMedCrossRefGoogle Scholar
  34. Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds. Oxford University Press, Oxford, pp 21–52Google Scholar
  35. Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  36. 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 102:124–136CrossRefGoogle Scholar
  37. Hacklander K, Arnold W (1999) Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota). Behav Ecol 10: 592–597CrossRefGoogle Scholar
  38. Hacklander K, Mostl E, Arnold W (2003) Reproductive suppression in female alpine marmots, Marmota marmota. Anim Behav 65:1133–1140CrossRefGoogle Scholar
  39. Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol Ecol 9:2163–2165PubMedCrossRefGoogle Scholar
  40. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474PubMedCrossRefGoogle Scholar
  41. Heller KG, Achmann R, Witt K (1993) Monogamy in the bat Rhinolophus sedulus? Z Saugetierkd 58:376–377Google Scholar
  42. 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 266:1021–1026CrossRefGoogle Scholar
  43. Horton NJ, Lipsitz SR (1999) Review of software to fit generalized estimating equation regression models. Am Stat 53:160–169CrossRefGoogle Scholar
  44. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  45. Johnsen A, Lifjeld JT, Rohde PA, Primmer CR, Ellegren H (1998) Sexual conflict over fertilizations: female bluethroats escape male paternity guards. Behav Ecol Sociobiol 43:401–408CrossRefGoogle Scholar
  46. Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492CrossRefGoogle Scholar
  47. Klinkitch M (1993) Untersuchugen zum paarungssystem des Alpenmurmeltiers, Marmota M. marmota mittels DNA fingerprinting. Ph.D. thesis, University of Munich, GermanyGoogle Scholar
  48. Kokko H, Johnstone R (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B 266:571–578CrossRefGoogle Scholar
  49. Komdeur J (2001) Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proc R Soc Lond B 268:2103–2111CrossRefGoogle Scholar
  50. Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22CrossRefGoogle Scholar
  51. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedGoogle Scholar
  52. Magnolon S (1999) Dispersion natale chez la marmotte alpine (Marmota marmota): modalités et effet de quelques facteurs proximaux. Ph.D. thesis, Université de ToursGoogle Scholar
  53. Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim Conserv 3:241–248CrossRefGoogle Scholar
  54. Marshall TC, Slate J, Kruuk LEB and Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  55. Matsubara M (2003) Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int J Primatol 24:1057–1075CrossRefGoogle Scholar
  56. Perrin C, Allainé D, Le Berre M (1993) Socio-spatial organization and activity distribution of the alpine marmot Marmota marmota: preliminary results. Ethology 93:21–30CrossRefGoogle Scholar
  57. 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 50:519–527CrossRefGoogle Scholar
  58. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, Berlin Heidelberg New YorkGoogle Scholar
  59. Plaistow SJ, Bollache L, Cezilly F (2003) Energetically costly precopulatory mate guarding in the amphipod Gammarus pulex: causes and consequences. Anim Behav 65:683–691CrossRefGoogle Scholar
  60. Price MV, Waser NM (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature 277:294–297CrossRefGoogle Scholar
  61. Queller D, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43: 258–275CrossRefGoogle Scholar
  62. R Development Core Team (2003) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  63. 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 35–56Google Scholar
  64. 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 3:347–353PubMedGoogle Scholar
  65. Rätti O, Hovi M, Lundberg A, Tegelström H, Alatalo RV (1995) Extra-paternity and male characteristics in the pied flycatcher. Behav Ecol Sociobiol 37:419–425CrossRefGoogle Scholar
  66. Raymond M, Rousset R (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  67. Reeve HK, Emlen ST (2000) Reproductive skew and group size: an N-person staying incentive model. Behav Ecol 11:640–647CrossRefGoogle Scholar
  68. Ribble DO (1991) The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166CrossRefGoogle Scholar
  69. Richardson PRK (1987) Aardwolf mating system: overt cuckoldry in an apparently monogamous mammal. S Afr J Sci 83:405–410Google Scholar
  70. Richardson DS, Burke T (2001) Extrapair paternity and variance in reproductive success related to breeding density in Bullock's orioles. Anim Behav 62:519–525CrossRefGoogle Scholar
  71. 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 10:2263–2273PubMedCrossRefGoogle Scholar
  72. Shellman Reeve JS, Reeve HK (2000) Extra-pair paternity as the result of reproductive transactions between paired mates. Proc R Soc Lond B 267:2543–2546CrossRefGoogle Scholar
  73. Shields WM (1983) Optimal inbreeding and the evolution of phylopatry. In: Swingland IR Greenwood PJ (eds) The ecology of animal movement. Clarendon, Oxford, pp 132–159Google Scholar
  74. Sillero-Zubiri C, Gottelli D, Macdonald DW (1996) Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav Ecol Sociobiol 38:331–340CrossRefGoogle Scholar
  75. Slagsvold T, Dale S (1994) Why do female pied flycatchers mate with already mated males: deception or restricted mate sampling? Behav Ecol Sociobiol 34:239–235CrossRefGoogle Scholar
  76. Slate J, Marshall TC and Pemberton JM (2000a) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808PubMedCrossRefGoogle Scholar
  77. 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 267:1657–1662CrossRefGoogle Scholar
  78. 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 8:1259–1272PubMedCrossRefGoogle Scholar
  79. Verhencamp SL (1983) Optimal degree of skew in reproductive societies. Am Zool 23:327–335Google Scholar
  80. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates and conflict. Ann Rev Ecol Syst 34:365–396CrossRefGoogle Scholar
  81. Williams GC (1975) Sex and evolution. Princeton University Press, PrincetonGoogle Scholar
  82. Wolff JO (1992) Parents suppress reproduction and stimulate dispersal in opposite-sex juvenile white-footed mice. Nature 359: 409–410PubMedCrossRefGoogle Scholar
  83. Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134PubMedCrossRefGoogle Scholar
  84. Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42:121–130PubMedCrossRefGoogle Scholar
  85. Zeh JA, Zeh DW (1996) The evolution of polyandry: I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717CrossRefGoogle Scholar
  86. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • A. Cohas
    • 1
  • N. G. Yoccoz
    • 2
  • A. Da Silva
    • 1
  • B. Goossens
    • 3
  • D. Allainé
    • 1
  1. 1.Laboratoire Biométrie et Biologie Evolutive, UMR CNRS 5558Université Claude Bernard Lyon 1Villeurbanne cedexFrance
  2. 2.Institute of BiologyUniversity of TromsøTromsøNorway
  3. 3.Biodiversity and Ecological Processes GroupCardiff School of Biosciences, Cardiff UniversityCardiffUK

Personalised recommendations