Conservation Genetics

, Volume 7, Issue 3, pp 371–382 | Cite as

Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota)

  • A. Da Silva
  • G. Luikart
  • N. G. Yoccoz
  • A. Cohas
  • D. Allainé


The relationship between individual genetic diversity and fitness-related traits are poorly understood in the wild. The availability of highly polymorphic molecular markers, such as microsatellites, has made research on this subject more feasible. We used three microsatellite-based measures of genetic diversity, individual heterozygosity H, mean d 2 and mean d 2 outbreeding to test for a relationship between individual genetic diversity and important fitness trait, juvenile survival, in a population of alpine marmots (Marmota marmota), after controlling for the effects of ecological, social and physiological parameters that potentially influence juvenile survival in marmots. Analyses were conducted on 158 juveniles, and revealed a positive association between juvenile survival and genetic diversity measured by mean H. No association was found with mean d 2 and with mean d 2 outbreeding. This suggests a fitness disadvantage to less heterozygous juveniles. The genetic diversity-fitness correlation (GDFC) was somewhat stronger during years with poor environmental conditions (i.e. wet summers). The stressful environmental conditions of this high mountain population might enhance inbreeding depression and make this association between genetic diversity and fitness detectable. Moreover the mating system, allowing extra pair copulation by occasional immigrants, as well as close inbreeding, favours a wide range of individual genetic diversity (mean H ranges from 0.125 to 1), which also may have facilitated the detection of the GDFC. The results further suggest that the observed GDFC is likely to be explained by the “local effect” hypothesis rather than by the “general effect” hypothesis.


heterozygosity inbreeding juvenile survival Marmota marmota microsatellites 


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We thank the Vanoise National Park for the access to the park, the region Rhône-Alpes, and the CNRS for their financial support. We are grateful to C. Miquel, M. Gaudeul for their help and support, to B. Goossens for his help in typing individuals, and to D. Coltman for helpful advice. We also thank Météo France for kindly providing us with weather data.


  1. Allainé D, Graziani L, Coulon J (1998) Postweaning mass gain in juvenile alpine marmots Marmota marmota. Oecologia 113: 370–376CrossRefGoogle 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. Behavioral Ecology 11: 507–514CrossRefGoogle Scholar
  3. Allainé D (2004) Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota. Behavioral Ecology 15: 987–1002Google Scholar
  4. Allainé D, Theuriau F (2004) Is there an optimal number of helpers in alpine marmot family groups?. Behavioral Ecology 15: 916–924CrossRefGoogle Scholar
  5. Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Soule ME (ed) Conservation Biology. Sinauer, Sunderland, MA, pp. 57–76Google Scholar
  6. Armitage KB, Downhower JF, Svendsen GE (1976) Seasonal changes in weights of marmots. American Midland Naturalist 96: 36–51CrossRefGoogle Scholar
  7. Arnold W (1990) The evolution of marmot sociality: I. Why disperse late? Behavioral Ecology and Sociobiology 27: 229–237Google Scholar
  8. Arnold W (1993) Social evolution in marmots and the adaptative value of joint hibernation. Verhandlungen der Deutschen Zoologischen Gesellschaft 86: 79–93Google Scholar
  9. Audo MC, Diehl WJ (1995) Effect of quantity and quality of environmental stress on multilocus heterozygosity-growth relationships in the eartworm, Eisenia fetida. Heredity 75: 98–105CrossRefGoogle Scholar
  10. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations?. Molecular Ecology 13: 3021–3031CrossRefPubMedGoogle Scholar
  11. Bibikov DI (1996) Taille, cycle annuel, et adaptation à l’été court des marmottes (Marmota). In: Le Berre M, Ramousse R, Le Guelte L (eds) Biodiversité chez les marmottes. International Marmot Network, Moscow, LyonGoogle Scholar
  12. Borsa P, Jousselin Y, Delay B (1992) Relationships between allozymic heterozygosity, body size, and survival to natural anoxic stress in the palourde Ruditapes decussatus L. (Bivalvia: Veneridae). Journal of experimental Marine Biology and Ecology 155: 169–181CrossRefGoogle Scholar
  13. Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88: 9–25CrossRefGoogle Scholar
  14. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  15. Coltman DW, Don Bowen W, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proceedings of the Royal Society of London (B) 265: 803–809CrossRefGoogle Scholar
  16. 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
  17. Coltman DW, Wilson K, Pilkington JG, Stear MJ, Pemberton JM (2001) A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitised population of Soay sheep. Parasitology 122: 571–582CrossRefPubMedGoogle Scholar
  18. Coltman DW, Slate J (2003) Microsatellite measures of inbreeding: A meta-analysis. Evolution 57: 971–983PubMedGoogle Scholar
  19. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014PubMedGoogle Scholar
  20. Coulson TN, Pemberton JM, Albon SD et al. (1998) Microsatellites reveal heterosis in red deer. Proceedings of the Royal Society of London (B) 265: 489–495CrossRefGoogle Scholar
  21. Coulson T, Albon S, Slate J, Pemberton J (1999) Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53:1951–1960CrossRefGoogle Scholar
  22. Crnokrak P, Roof DA (1999) Inbreeding depression in the wild. Heredity 83: 260–270CrossRefPubMedGoogle Scholar
  23. Danzmann RG, Ferguson MM, Allendorf FW (1988) Heterozygosity and components of fitness in a strain of rainbow trout. Biology Journal of the Linnean Society 33:285–304CrossRefGoogle Scholar
  24. David P (1998) Heterozygosity-fitness correlations: new perspective on old problems. Heredity 80: 531–537PubMedCrossRefGoogle Scholar
  25. Duarte L, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638–645PubMedGoogle Scholar
  26. Dudash MR (1990) Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129–1139CrossRefGoogle Scholar
  27. Farand E, Allainé D, Coulon J (2002) Variation in survival rates for the alpine marmot (Marmota marmota): effects of sex, age, year, and climatic factors. Canadian Journal of Zoology 80: 342–349CrossRefGoogle Scholar
  28. Florant GL, Hester L, Ameenuddin S, Rintoul DA (1993) The effect of a low essential fatty acid diet on hibernation in marmots. American Journal of Physiology 264: 747–753Google Scholar
  29. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717CrossRefPubMedGoogle Scholar
  30. Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. American Journal of Physiology 292: 897–901Google Scholar
  31. Goossens B, Graziani L, Waits L et al. (1998) Extra-pair paternity in the monogamous alpine marmot revealed by nuclear DNA microsatellite analysis. Behavioral Ecology and Sociobiology 43: 281–288CrossRefGoogle Scholar
  32. Goossens B, Chikhi L, Taberlet P, Waits LP, Allainé D (2001) Microsatellite analysis of genetic variation among and within Alpine marmot populations in the French Alps. Molecular Ecology 10: 41–52CrossRefPubMedGoogle Scholar
  33. Goudet J, Keller L (2002) The correlation between inbreeding and fitness: does allele size matter?. Trends in Ecology and Evolution 5:201–202CrossRefGoogle Scholar
  34. Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European Sciurid species (Marmota marmota, Spermophilus citellus). Molecular Ecology 9:2163–2165CrossRefPubMedGoogle Scholar
  35. Hansson B, Bensch S, Hasselquist D, Akesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proceedings of the Royal Society of London (B) 268: 1287–1291CrossRefGoogle Scholar
  36. Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology 11:2467–2474CrossRefPubMedGoogle Scholar
  37. Hansson B, Westerdahl H, Hasselquist D, Akesson M, Bensch S (2004) Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers?. Evolution 58: 870–879PubMedGoogle Scholar
  38. Hedrick P, Fredrickson R, Ellegren H (2001) Evaluation of d2, a microsatellite measure of inbreeding and outbreeding, in wolves with a known pedigree. Evolution 55: 1256–1260PubMedGoogle Scholar
  39. Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theoretical Population Biology 38: 226–239Google Scholar
  40. Hoffman JI, Boyd IL, Amos W (2004) Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella. Evolution 58, 2087–2099PubMedGoogle Scholar
  41. Höglund J, Piertney SB, Alatalo RV et al. (2002) Inbreeding depression and male fitness in black grouse. Proceedings of the Royal Society of London (B) 269, 711–715CrossRefGoogle Scholar
  42. Houle D, (1989) Allozyme associated heterozis in Drosophila melanogaster. Genetics 123, 789–801PubMedGoogle Scholar
  43. Ihaka R, Gentleman R, (1996) R: a language for data analysis and graphics. Journal of computational and graphical statistics 5, 299–341CrossRefGoogle Scholar
  44. Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11, 424–429CrossRefGoogle Scholar
  45. Jorgenson JT, Festa-Bianchet M, Gaillard JM, Wishart WD (1997) Effects of age, sex, disease and density on survival of bighorn sheep. Ecology 78: 1019–1032Google Scholar
  46. Kashi Y, Soller M, (1999) Functional roles of microsatellites and minisatellites. In: Goldstein DB, Schlötterer C (eds), Microsatellites Evolution and Applications. Oxford University Press, New York, pp.10–23Google Scholar
  47. Klinkicht M (1993) Untersuchungen zum paanungssystem des alpenmurmeltieres, Marmota m. marmota, mittels DNA fingerprinting. Ph.D. Thesis, University of MünchenGoogle Scholar
  48. Lacy RC, (1993) Impacts of inbreeding in natural and captive populations of vertebrates: implications for conservation. Persepectives In Biology And Medicine 36: 480–496Google Scholar
  49. Lesbarrères D, Primmer CR, Laurila A, Merilä J (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Molecular Ecology 14: 311–323CrossRefPubMedGoogle Scholar
  50. Loison A (1995) Approche intra- et inter-spécifiques de la dynamique des populations: l’exemple du chamois. Ph.D. Thesis, Université Lyon1Google Scholar
  51. Markert JA, Grant PR, Grant BR et al. (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin’s ground finches (Geospiza fortis and G. scandens). Heredity 92, 306–315CrossRefPubMedGoogle Scholar
  52. McCullagh P, Nelder JA, (1989) Generalized linear Models. Chapman and Hall, LondonGoogle Scholar
  53. McRae AF, McEwan JC, Dodds KG et al. (2002) Linkage disequilibrium in domestic sheep. Genetics 160: 1113–1122PubMedGoogle Scholar
  54. Meagher S, Penn DJ, Potts WK (1997) Male-male competition magnifies inbreeding depression in wild house mice. Proceedings of the National Academy of Sciences of the USA 7: 3324–3333Google Scholar
  55. Mitton JB (1993) Theory and data pertinent to the relationship between heterozygosity and fitness. In: The Natural History Of Inbreeding And Outbreeding Theoritical And Empirical Perspectives By Thornhill, 17–41Google Scholar
  56. Mysterud ANC, Stenseth NG, Yoccoz R, Langvatn I, Steinheim G (2001) Nonlinear effects of large-scale climatic variability on wild and domestic herbivores. Nature 410, 1096–1099CrossRefPubMedGoogle Scholar
  57. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590PubMedGoogle Scholar
  58. Otah T (1971) Associative overdominance caused by linked detrimental mutations. Genetical Research (Cambridge) 18, 277–286Google Scholar
  59. Ozenda P, (1985) La végétation de la chaine alpine dans l’espace montagnard européen. Masson, ParisGoogle Scholar
  60. Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology and Evolution 19, 613–615CrossRefPubMedGoogle Scholar
  61. Perrin C, Coulon J, Le Berre M (1993) Social behaviour of alpine marmots (Marmota marmota): seasonal, group and individual variability. Canadian Journal of Zoology 71, 1945–1953CrossRefGoogle Scholar
  62. Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proceedings of the Royal Society of London (B) 247: 203–210CrossRefGoogle Scholar
  63. Queller DC, Strassman JE, Hughes CR (1993) Microsatellites and kinship. Trends in Ecology and Evolution 8, 285–288CrossRefGoogle 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. Molecular Ecology 3, 347–353PubMedCrossRefGoogle Scholar
  65. Raymond M, Rousset F (1995) GENEPOP (version 3.3): a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249Google Scholar
  66. Reich DE, Cargill M, Bolk S et al. (2001) Linkage disequilibrium in the human genome. Nature 411, 199–204CrossRefPubMedGoogle Scholar
  67. Rossiter SJ, Jones G, Ransome RD, Barratt EM (2001) Outbreeding increase offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proceedings of the Royal Society of London (B) 268, 1055–1061CrossRefGoogle Scholar
  68. Rowe G, Beebee TJC (2001) Fitness and microsatellite diversity estimates were not correlated in two outbred anuran populations. Heredity 87, 558–565CrossRefPubMedGoogle Scholar
  69. Schwartz OA, Armitage KB, Van Vuren D (1998) A 32-year demography of yellow-bellied marmots (Marmota flaviventris). Journal of Zoology (London) 246, 337–346CrossRefGoogle Scholar
  70. Seddon N, Amos W, Mulder RA, Tobias JA (2004), Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird. Proceedings of the Royal Society of London (B) 271, 1823–1829CrossRefGoogle Scholar
  71. Slate J, Kruuk LEB, Marshall TC, Pemberton JM (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proceedings of the Royal Society of London (B) 267, 1657–1662CrossRefGoogle Scholar
  72. Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. Journal of Evolutionary Biology 15, 20–31CrossRefGoogle Scholar
  73. Slate J, David P, Dodds KG et al. (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93, 255–265CrossRefPubMedGoogle Scholar
  74. Steele BM, Hogg JT (2003) Measuring individual quality in conservation and behavior. In: Festa-Bianchet M, Apollonio M, (eds), Animal behaviour and wildlife conservation. Island Press, pp. 243–271Google Scholar
  75. Tsitrone A, Rousset F, David P (2001) Heterosis, marker mutational processes and population inbreeding history. Genetics 159, 1845–1859PubMedGoogle Scholar
  76. Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133: 737–749PubMedGoogle Scholar
  77. Van Horne B, Olson GS, Schooley RL, Com JG , Burnham KP (1997) Effects of drought and prolonged winter on Townsend’s grounds squirrel demography in schrubsteppe habitats. Ecological Monographs 67, 295–315Google Scholar
  78. Weir BS, Cockerham CC (1973) Mixed self and random mating at two loci. Genetical Reserach (Cambridge) 21, 247–262Google Scholar
  79. Wood BC, Armitage KB (2002) Effect of food supplementation on juvenile growth and survival in Marmota flaviventris. Journal of Mammalogy 84, 903–914CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • A. Da Silva
    • 1
  • G. Luikart
    • 2
  • N. G. Yoccoz
    • 3
  • A. Cohas
    • 1
  • D. Allainé
    • 1
  1. 1.Laboratoire de Biométrie et Biologie EvolutiveVilleurbanne cedexFrance
  2. 2.Laboratoire d’Ecologie Alpine (Population Genomics and Biodiversity)Grenoble, Cedex 09France
  3. 3.Institute of BiologyUniversity of TromsøTromsøNorway

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