Behavioral Ecology and Sociobiology

, Volume 57, Issue 3, pp 240–244

Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar)

Original Article

Abstract

Inbreeding has negative effects on individual and population performances. Therefore, enhancement of offspring genetic diversity is believed to play a major role in shaping mating systems. However, no study has clearly separated the direct effect of having multiple partners from the indirect effect of having more outbred offspring on the resulting reproductive success of individuals in the wild. In this study, we report significant associations between both multiple mating and within-individual genetic diversity of offspring, and an increased reproductive success of wild female Atlantic salmon, Salmo salar. Specifically, we found that females with a higher number of mates also have more outbred offspring (within-individuals), and that both of these characteristics increased their reproductive success expressed in terms of offspring surviving when combining all freshwater juvenile stages. Our findings also indicate that determinants of fitness are different among sexes as within-individual offspring genetic diversity was not a strong predictor of male reproductive success, while the number of mates was important. We also show that females mated with more outbred males than on average, which potentially increased their chances of producing outbred offspring. These results therefore suggest that there could be more important indirect genetic benefits of multiple mating for females than for males.

Keywords

Multiple paternity Genetic benefits Reproductive success Internal relatedness Mate choice 

References

  1. Acedevo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Disease susceptibility in California sea lions. Nature 422:35PubMedGoogle Scholar
  2. Aeschlimann PB, Haberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54:119–126Google Scholar
  3. Amos W, Worthington Wilmer J, Fullard K, Burg T, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2028PubMedGoogle Scholar
  4. Aubin-Horth N, Dodson JJ (2004) Influence of individual body size and variable thresholds on the incidence of a sneaker male reproductive tactic in Atlantic salmon. Evolution 58:136–144PubMedGoogle Scholar
  5. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368Google Scholar
  6. Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615CrossRefPubMedGoogle Scholar
  7. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65Google Scholar
  8. Brown J, Brown E (1998) Are inbred offspring less fit? Survival in a natural population of Mexican jays. Behav Ecol 9:60–63CrossRefGoogle Scholar
  9. Coltman DW, Slate J (2003) Microsatellites measures of inbreeding: a meta-analysis. Evolution 57:971–983PubMedGoogle Scholar
  10. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270PubMedGoogle Scholar
  11. Duchesne P, Godbout MH, Bernatchez L (2002) PAPA (package for the analysis of parental allocation): a computer program for simulated and real parental allocation. Mol Ecol Notes 2:191–193Google Scholar
  12. 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
  13. Garant D, Dodson JJ, Bernatchez L (2000) Ecological determinants and temporal stability of within-river population structure in Atlantic salmon (Salmo salar L.). Mol Ecol 9:615–628PubMedGoogle Scholar
  14. Garant D, Dodson JJ, Bernatchez L (2001) A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). J Hered 92:137–145PubMedGoogle Scholar
  15. Garant D, Fontaine P-M, Good SP, Dodson JJ, Bernatchez L (2002) The influence of male parental identity on growth and survival of offspring in Atlantic salmon (Salmo salar). Evol Ecol Res 4:537–549Google Scholar
  16. Garant D, Dodson JJ, Bernatchez L (2003) Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.). Evolution 57:1133–1141PubMedGoogle Scholar
  17. Griffiths SW, Armstrong JD (2001) The benefits of genetic diversity outweigh those of kin association in a territorial animal. Proc R Soc Lond B 268:1293–1296PubMedGoogle Scholar
  18. Heath DD, Bryden CA, Shrimpton JM, Iwama GK, Kelly J, Heath JW (2002) Relationships between heterozygosity, allelic distance (d2), and reproductive traits in chinook salmon, Oncorhynchus tshawytscha. Can J Fish Aquat Sci 59:77–84CrossRefGoogle Scholar
  19. Hohoff C, Franzen K, Sachser N (2003) Female choice in a promiscuous wild guinea pig, the yellow-toothed cavy (Galea musteloides). Behav Ecol Sociobiol 53:341–349Google Scholar
  20. Joron M, Brakefield PM (2003) Captivity masks inbreeding effects on male mating success in butterflies. Nature 424:191–194PubMedGoogle Scholar
  21. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  22. Kellogg KA (1999) Salmon on the edge. Trends Ecol Evol 14:45–46CrossRefGoogle Scholar
  23. Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc Lond B 270:653–664CrossRefPubMedGoogle Scholar
  24. Kruuk LEB, Sheldon BC, Merilä J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond B 269:1581–1589CrossRefPubMedGoogle Scholar
  25. 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 268:1279–1285CrossRefPubMedGoogle Scholar
  26. Lehmann L, Perrin N (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat 162:638–652CrossRefPubMedGoogle Scholar
  27. McGinnity P, Prodöhl P, Ferguson A, Hynes R, Ó Maoiléidigh N, Baker N, Cotter D, O’Hea B, Cooke D, Rogan G, Taggart J Cross T (2003) Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc R Soc Lond B 270:2443–2450CrossRefPubMedGoogle Scholar
  28. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206CrossRefGoogle Scholar
  29. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275Google Scholar
  30. Rossiter SJ, Jones G, Ransome RD, Barratt EM (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proc R Soc Lond B 268:1055–1061CrossRefPubMedGoogle Scholar
  31. Stabell OB (1984) Homing and olfaction in salmonids: a critical review with special reference to the Atlantic salmon. Biol Rev 59:333–388Google Scholar
  32. Taggart JB, McLaren IS, Hay DW, Webb JH, Youngson AF (2001) Spawning success in Atlantic salmon (Salmo salar L.): a long-term DNA profiling-based study conducted in a natural stream. Mol Ecol 10:1047–1060CrossRefPubMedGoogle Scholar
  33. Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207CrossRefGoogle Scholar
  34. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73CrossRefPubMedGoogle Scholar
  35. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 136–179Google Scholar
  36. VSN Intl (2003) Genstat version 7.1.VSN International Ltd, OxfordGoogle Scholar
  37. Wang S, Hard JJ, Utter F (2002) Salmonid inbreeding: a review. Rev Fish Biol Fish 11:301–319Google Scholar
  38. Yasui Y (1998) The “genetic benefits” of female multiple mating reconsidered. Trends Ecol Evol 13:246–250CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Dany Garant
    • 1
    • 2
  • Julian J. Dodson
    • 1
  • Louis Bernatchez
    • 1
  1. 1.Département de BiologieUniversité LavalLavalCanada
  2. 2.Edward Grey Institute, Department of ZoologyUniversity of OxfordOxfordUK

Personalised recommendations