Abstract
Assuming that a male’s genetic characteristics affect those of his offspring, extra-pair copulation has been hypothesized to increase heterozygosity of the progeny—the “genetic compatibility” hypothesis—and the genetic diversity within litters—the “genetic diversity” hypothesis. We tested these two hypotheses in the alpine marmot (Marmota marmota), a socially monogamous mammal showing a high rate of extra-pair paternity (EPP). In a first step, we tested the assumption that a male’s genetic characteristics (heterozygosity and genetic similarity to the female) affect those of his offspring. Genetic similarity between parents influenced offspring heterozygosity, offspring genetic similarity to their mother, and litter genetic diversity. The father’s heterozygosity also influenced litter genetic diversity but did not affect offspring heterozygosity. Hence, heterozygosity seems not to be heritable in the alpine marmot. In a second step, we compared genetic characteristics of extra-pair young (EPY) and within-pair young (WPY). EPY were less genetically similar to their mother but not more heterozygous than WPY. EPY siblings were also less genetically similar than their WPY half siblings. Finally, the presence of EPY promoted genetic diversity within the litter. Thus, our data support both the “genetic compatibility” and the “genetic diversity” hypotheses. We discuss further investigations needed to determine the primary causes of EPP in this species.
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References
Allainé D (2004) Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota. Behav Ecol 15:997–1002
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
Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 57–76
Amos W, Worthington-Wilmer J, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001a) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027
Amos W, Wilmer JW, Kokko H (2001b) Do female grey seals select genetically diverse mates? Anim Behav 62:157–164
Aparicio JM, Cordero PJ, Veiga JP (2001) A test of the hypothesis of mate choice based on heterozygosity in the spotless starling. Anim Behav 62:1001–1006
Arnold W (1990) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237
Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154
Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031
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
Bensch S, Hasselquist D, Schantz T (1994) Genetic similarity between parents predicts hatching failure: nonincestuous inbreeding in the great reed warbler? Evolution 48:317–326
Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic, London
Birkhead TR, Møller AP (1995) Extra-pair copulation and extra-pair paternity in birds. Anim Behav 49:843–848
Blomqvist D, Andersson M, Kupper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Szekely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615
Blouin M (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511
Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65
Brown JL, Eklund A (1994) Kin recognition and the major histocompatibility complex: an integrative review. Am Nat 143:435–461
Byrne P, Roberts J (2000) Does multiple paternity improve fitness of the frog Crinia georgiana? Evolution 54:968–973
Charmantier A, Blondel J, Perret P, Lambrechts MM (2004) Do extra-pair paternities provide genetic benefits for female blue tits (Parus caeruleus)? J Avian Biol 35:524–532
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
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
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
Da Silva A, Luikart G, Allainé D, Gautier PT, Taberlet P, Pompanon F (2003) Isolation and characterization of microsatellites in European alpine marmots (Marmota marmota). Mol Ecol Notes 3:189–190
David P (1998) Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80:531–537
Dunn PO, Robertson RJ, Michaud-Freeman D, Boag PT (1994) Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35:273–281
Eimes JA, Parker PG, Brown JL, Brown ER (2005) Extrapair fertilization and genetic similarity of social mates in the Mexican jay. Behav Ecol 16:456–460
Farr JA (1980) Social behavior patterns as determinants of reproductive success in the guppy, Poecilia reticulata (Pisces: Poeciliidae). Behaviour 74:38–91
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
Fuchs S, Schade V (1994) Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155–168
Goossens B, Coulon J, Allainé D, Graziani L, Bel MC, Taberlet P (1996) Immigration of a pregnant female in an alpine marmot family group: behavioural and genetic data. C R Acad Sci (Paris) 319:241–246
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
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
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
Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol Ecol 9:2163–2165
Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11:2467–2474
Hansson B, Bensch S, Hasselquist D, Åkesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc R Soc Lond B 268:1287–1291
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
Hoogland J (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin’s finches. Evolution 56:1229–1239
Kempenaers B, Verheyen GR, Dhondt AA (1997) Extra-pair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492
Kleven O, Lifjeld JT (2005) No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus). Behav Ecol 16:561–565
Klinkicht M (1993) Untersuchugen zum paarungssystem des Alpenmurmeltiers, Marmota M. marmota mittels DNA fingerprinting. Ph.D. thesis, University of Munich, Germany
Landry C, Garant D, Duchesne P, Bernatchez L (2001) ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc R Soc Lond B 268:1279–1285
Leisler B, Beier J, Staudter H, Wink M (2000) Variation in extra-pair paternity in the polygynous Great Reed Warbler (Acrocephalus arundinaceus). J Ornithol 141:77–84
Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc Lond B 265:221–225
Loman J, Madsen T, Håkansson T (1988) Increased fitness from multiple mating and genetic heterogeneity: a model of a possible mechanism. Oikos 52:69–72
Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766
Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature 355:440–441
Marshall RC, Buchanan KL, Catchpole CK (2003) Sexual selection and individual genetic diversity in a songbird. Proc R Soc Lond B 270:S248–S250
Masters BS, Hicks BG, Scott Johnson L, Erb LA (2003) Genotype and extra-pair paternity in the house wren: a rare-male effect? Proc R Soc Lond B 270:1393–1397
Mateo JM (2006) The nature and representation of individual recognition odors in Belding’s ground squirrels. Anim Behav 71:141–154
Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559
Mitton JB (1993) Theory and data pertinent to the relationship between heterozygosity and fitness. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. University of Chicago Press, Chicago, pp 17–41
Møller AP, Birkhead TR (1993) Cuckoldry and sociality: a comparative study of birds. Am Nat 142:118–140
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38
Oldroyd B, Clifton M, Wongsiri S, Rinderer T, Sylvester H, Crozier R (1997) Polyandry in the genus Apis, particularly Apis andreniformis. Behav Ecol Sociobiol 40:17–26
Olsson M, Gullberg A, Tegelstrom H, Madsen T, Shine R (1994) Can female adders multiply? Nature 369:528
Otter K, Ratcliffe L, Michaud D, Boag PT (1998) Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 43:25–36
Penn D, Potts WK (1998) Untrained mice discriminate MHC-determined odours. Physiol Behav 63:235–243
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
Pinheiro JC, Bates DM (2002) Mixed-effects models in S and S-plus. Springer, Berlin Heidelberg New York
Pusey AE, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206
Queller D, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
R Development Core Team (2003) R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing
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
Raymond M, Rousset R (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Richardson D, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc Lond B 272:759–767
Ridley M (1993) Clutch size and mating frequency in parasitic Hymenoptera. Am Nat 142:893–910
Rousset F (2002) Inbreeding and relatedness coefficients: what do we measure? Heredity 88:371–380
Schmoll T, Quellmalz A, Dietrich V, Winkel W, Epplen JT, Lubjuhn T (2005) Genetic similarity between pair mates is not related to extrapair paternity in the socially monogamous coal tit. Anim Behav 69:1013–1022
Sheldon B, Ellegren H (1996) Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B 263:1017–1021
Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. J Evol Biol 15:20–31
Slate J, Dodds K, Veenvliet B, Glass B, Broad T, McEwan J (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265
Strohbach S, Curio E, Bathen A, Epplen JT, Lubjuhn T (1998) Extra-pair paternity in the great tit (Parus major): a test of the ‘good genes’ hypothesis. Behav Ecol 9:296–388
Tregenza T, Wedell N (1998) Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52:1726–1730
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage. Mol Ecol 9:1013–1027
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine–Atherton, Chicago, pp 136–179
Van de Casteele T, Galbusera P, Matthysen E (2001) A comparison of microsatellite-based pairwise relatedness estimators. Mol Ecol 10:1539–1549
Venables WN, Ripley BD (2002) Modern Applied Statistics with S 4th edn. Springer, Berlin Heidelberg New York
Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates and conflict. Annu Rev Ecol Syst 34:365–396
Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369
Williams GC (1975) Sex and evolution. Princeton University Press, Princeton
Yasui Y (1998) The “genetic benefits” of female multiple mating reconsidered. Trends Ecol Evol 13:246–250
Zeh J, Zeh D (1996) The evolution of polyandry: I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717
Zeh J, Zeh D (1997) The evolution of polyandry II: Post-copulatory defenses against genetic compatibility. Proc R Soc Lond B 264:69–75
Acknowledgements
We thank all students involved in the trapping of alpine marmots at La Sassière and Benoit Goossens for the typing of marmots, Mark Hewison for editing the English, and the authorities of the Vanoise National Park for allowing us to work in the Grande Sassière Nature Reserve. Finally, we thank Daniel Chessel for statistical advice. 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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Cohas, A., Yoccoz, N.G. & Allainé, D. Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behav Ecol Sociobiol 61, 1081–1092 (2007). https://doi.org/10.1007/s00265-006-0341-7
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DOI: https://doi.org/10.1007/s00265-006-0341-7