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

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Abstract

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.

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References

  • Allainé D, Graziani L, Coulon J (1998) Postweaning mass gain in juvenile alpine marmots Marmota marmota. Oecologia 113: 370–376

    Article  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. Behavioral Ecology 11: 507–514

    Article  Google Scholar 

  • Allainé D (2004) Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota. Behavioral Ecology 15: 987–1002

    Google Scholar 

  • Allainé D, Theuriau F (2004) Is there an optimal number of helpers in alpine marmot family groups?. Behavioral Ecology 15: 916–924

    Article  Google Scholar 

  • Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Soule ME (ed) Conservation Biology. Sinauer, Sunderland, MA, pp. 57–76

    Google Scholar 

  • Armitage KB, Downhower JF, Svendsen GE (1976) Seasonal changes in weights of marmots. American Midland Naturalist 96: 36–51

    Article  Google Scholar 

  • Arnold W (1990) The evolution of marmot sociality: I. Why disperse late? Behavioral Ecology and Sociobiology 27: 229–237

    Google Scholar 

  • Arnold W (1993) Social evolution in marmots and the adaptative value of joint hibernation. Verhandlungen der Deutschen Zoologischen Gesellschaft 86: 79–93

    Google Scholar 

  • 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: 98–105

    Article  Google Scholar 

  • Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations?. Molecular Ecology 13: 3021–3031

    Article  PubMed  CAS  Google Scholar 

  • 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, Lyon

    Google Scholar 

  • 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: 169–181

    Article  Google Scholar 

  • Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88: 9–25

    Article  Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, Chicago

    Google Scholar 

  • 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: 803–809

    Article  CAS  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 

  • 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: 571–582

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Slate J (2003) Microsatellite measures of inbreeding: A meta-analysis. Evolution 57: 971–983

    PubMed  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014

    PubMed  CAS  Google Scholar 

  • Coulson TN, Pemberton JM, Albon SD et al. (1998) Microsatellites reveal heterosis in red deer. Proceedings of the Royal Society of London (B) 265: 489–495

    Article  CAS  Google Scholar 

  • Coulson T, Albon S, Slate J, Pemberton J (1999) Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53:1951–1960

    Article  Google Scholar 

  • Crnokrak P, Roof DA (1999) Inbreeding depression in the wild. Heredity 83: 260–270

    Article  PubMed  Google Scholar 

  • Danzmann RG, Ferguson MM, Allendorf FW (1988) Heterozygosity and components of fitness in a strain of rainbow trout. Biology Journal of the Linnean Society 33:285–304

    Article  Google Scholar 

  • David P (1998) Heterozygosity-fitness correlations: new perspective on old problems. Heredity 80: 531–537

    Article  PubMed  Google Scholar 

  • Duarte L, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638–645

    PubMed  CAS  Google Scholar 

  • 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: 1129–1139

    Article  Google Scholar 

  • 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: 342–349

    Article  Google Scholar 

  • 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: 747–753

    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 

  • Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. American Journal of Physiology 292: 897–901

    Google Scholar 

  • 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: 281–288

    Article  Google Scholar 

  • 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: 41–52

    Article  PubMed  CAS  Google Scholar 

  • Goudet J, Keller L (2002) The correlation between inbreeding and fitness: does allele size matter?. Trends in Ecology and Evolution 5:201–202

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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: 1287–1291

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hansson B, Westerdahl H, Hasselquist D, Akesson M, Bensch S (2004) Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers?. Evolution 58: 870–879

    PubMed  Google Scholar 

  • 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: 1256–1260

    PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theoretical Population Biology 38: 226–239

    Google Scholar 

  • 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, 2087–2099

    PubMed  Google Scholar 

  • 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, 711–715

    Article  Google Scholar 

  • Houle D, (1989) Allozyme associated heterozis in Drosophila melanogaster. Genetics 123, 789–801

    PubMed  CAS  Google Scholar 

  • Ihaka R, Gentleman R, (1996) R: a language for data analysis and graphics. Journal of computational and graphical statistics 5, 299–341

    Article  Google Scholar 

  • Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends in Ecology and Evolution 11, 424–429

    Article  Google Scholar 

  • Jorgenson JT, Festa-Bianchet M, Gaillard JM, Wishart WD (1997) Effects of age, sex, disease and density on survival of bighorn sheep. Ecology 78: 1019–1032

    Google Scholar 

  • 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.10–23

    Google Scholar 

  • Klinkicht M (1993) Untersuchungen zum paanungssystem des alpenmurmeltieres, Marmota m. marmota, mittels DNA fingerprinting. Ph.D. Thesis, University of München

  • Lacy RC, (1993) Impacts of inbreeding in natural and captive populations of vertebrates: implications for conservation. Persepectives In Biology And Medicine 36: 480–496

    Google Scholar 

  • Lesbarrères D, Primmer CR, Laurila A, Merilä J (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Molecular Ecology 14: 311–323

    Article  PubMed  Google Scholar 

  • Loison A (1995) Approche intra- et inter-spécifiques de la dynamique des populations: l’exemple du chamois. Ph.D. Thesis, Université Lyon1

  • 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, 306–315

    Article  PubMed  CAS  Google Scholar 

  • McCullagh P, Nelder JA, (1989) Generalized linear Models. Chapman and Hall, London

    Google Scholar 

  • McRae AF, McEwan JC, Dodds KG et al. (2002) Linkage disequilibrium in domestic sheep. Genetics 160: 1113–1122

    PubMed  CAS  Google Scholar 

  • 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: 3324–3333

    Google Scholar 

  • 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, 17–41

  • 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, 1096–1099

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Otah T (1971) Associative overdominance caused by linked detrimental mutations. Genetical Research (Cambridge) 18, 277–286

    Google Scholar 

  • Ozenda P, (1985) La végétation de la chaine alpine dans l’espace montagnard européen. Masson, Paris

    Google Scholar 

  • Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology and Evolution 19, 613–615

    Article  PubMed  Google Scholar 

  • 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, 1945–1953

    Article  Google Scholar 

  • Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proceedings of the Royal Society of London (B) 247: 203–210

    Article  Google Scholar 

  • Queller DC, Strassman JE, Hughes CR (1993) Microsatellites and kinship. Trends in Ecology and Evolution 8, 285–288

    Article  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. Molecular Ecology 3, 347–353

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 3.3): a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249

    Google Scholar 

  • Reich DE, Cargill M, Bolk S et al. (2001) Linkage disequilibrium in the human genome. Nature 411, 199–204

    Article  PubMed  CAS  Google Scholar 

  • 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, 1055–1061

    Article  CAS  Google Scholar 

  • Rowe G, Beebee TJC (2001) Fitness and microsatellite diversity estimates were not correlated in two outbred anuran populations. Heredity 87, 558–565

    Article  PubMed  CAS  Google Scholar 

  • Schwartz OA, Armitage KB, Van Vuren D (1998) A 32-year demography of yellow-bellied marmots (Marmota flaviventris). Journal of Zoology (London) 246, 337–346

    Article  Google Scholar 

  • 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, 1823–1829

    Article  Google Scholar 

  • 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, 1657–1662

    Article  CAS  Google Scholar 

  • Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. Journal of Evolutionary Biology 15, 20–31

    Article  Google Scholar 

  • 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, 255–265

    Article  PubMed  CAS  Google Scholar 

  • 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. 243–271

    Google Scholar 

  • Tsitrone A, Rousset F, David P (2001) Heterosis, marker mutational processes and population inbreeding history. Genetics 159, 1845–1859

    PubMed  CAS  Google Scholar 

  • Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133: 737–749

    PubMed  CAS  Google Scholar 

  • 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, 295–315

    Google Scholar 

  • Weir BS, Cockerham CC (1973) Mixed self and random mating at two loci. Genetical Reserach (Cambridge) 21, 247–262

    CAS  Google Scholar 

  • Wood BC, Armitage KB (2002) Effect of food supplementation on juvenile growth and survival in Marmota flaviventris. Journal of Mammalogy 84, 903–914

    Article  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard Lyon I, 43 Bd du 11 novembre 1918, 69622, Villeurbanne cedex, France

    A. Da Silva, A. Cohas & D. Allainé

  2. Laboratoire d’Ecologie Alpine (Population Genomics and Biodiversity), UMR CNRS 5553, Université J. Fourier, BP53, F-38041, Grenoble, Cedex 09, France

    G. Luikart

  3. Institute of Biology, University of Tromsø, 9037, Tromsø, Norway

    N. G. Yoccoz

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  1. A. Da Silva
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  2. G. Luikart
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  3. N. G. Yoccoz
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  4. A. Cohas
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  5. D. Allainé
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Correspondence to A. Da Silva.

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Silva, A.D., Luikart, G., Yoccoz, N.G. et al. Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota). Conserv Genet 7, 371–382 (2006). https://doi.org/10.1007/s10592-005-9048-y

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