Skip to main content
SpringerLink
Log in

Do dominants have higher heterozygosity? Social status and genetic variation in brown trout, Salmo trutta

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

A key question of evolutionary importance is what factors influence who becomes dominant. Individual genetic variation has been found to be associated with several fitness traits, including behaviour. Could it also be a factor influencing social dominance? We investigated the association between social status and the amount of intra-individual genetic variation in juvenile brown trout (Salmo trutta). Genetic variation was estimated using 12 microsatellite loci. Dominant individuals had higher mean heterozygosity than subordinates in populations with the longest hatchery background. Heterozygosity–heterozygosity correlations did not find any evidence of inbreeding; however, single-locus analysis revealed four loci that each individually differed significantly between dominant and subordinate fish, thus giving more support to local than general effect as the mechanism behind the observed association between genetic diversity and a fitness-associated trait. We did not find any significant relation between mean d 2 and social status, or internal relatedness and social status. Our results suggest that individual genetic variation can influence dominance relations, but manifestation of this phenomenon may depend on the genetic background of the population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Disease susceptibility in Californian sea lions. Nature 422:35

    Article  PubMed  CAS  Google Scholar 

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  PubMed  CAS  Google Scholar 

  • Allendorf FW, Phelps SR (1980) Loss of genetic variation in a hatchery stock of cutthroat trout. Trans Am Fish Soc 109:537–543

    Article  Google Scholar 

  • Allison PD (1999) Logistic regression using the SAS system. Theory and application. SAS Institute Inc., Cary, NC

    Google Scholar 

  • Altukhov YP, Salmenkova EA, Omelchenko VT (2000) Salmonid fishes. In: Carvalho GR, Thorpe JE (eds) Population biology, genetics and management (English translation). Blackwell, Oxford

  • Amos W, Worthington-Wilmer J, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027

    Article  CAS  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

    Google Scholar 

  • Bailey J, Alanärä A, Brännäs E (2000) Methods for assessing social status in Arctic charr. J Fish Biol 57:258–261

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bean K, Amos W, Pomeroy PP, Twiss D, Coulson TN, Boyd IL (2004) Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus). Mol Ecol 13:2365–2370

    Article  PubMed  CAS  Google Scholar 

  • Bierne N, Launey S, Naciri-Graven Y, Bonhomme F (1998) Early effects of inbreeding as revealed by microsatellite analysed on Ostrea edulis larvae. Genetics 148:1893–1906

    PubMed  CAS  Google Scholar 

  • Borrell YJ, Pineda H, McCarthy I, Vázquez, Sánchez JA, Lizana GB (2004) Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L. Heredity 92:585–593

    Article  PubMed  CAS  Google Scholar 

  • Cairney M, Taggart JB, Hoyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Mol Ecol 9:2175–2178

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D (1991) The apparent selection on neutral marker loci in partially inbreeding populations. Genet Res 57:159–175

    Article  Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1986) Great expectations: dominance, breeding success and offspring se ratios in red deer. Anim Behav 34:460–471

    Article  Google Scholar 

  • Coltman DW, Bowen W, Wright JM (1998) Birth weight and neontal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc R Soc Lond B 265:803–809

    Article  CAS  Google Scholar 

  • Coulson TN, Pemberton JM, Albon SD, Beaumont M, Marshall TC, Slate J, Guinnes FE, Glutton-Brock TH (1998) Microsatellites reveal heterosis in red deer. Proc R Soc Lond B 265:489–495

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Crozier WW (1998) Genetic implications of hatchery rearing in Atlantic salmon: effects of rearing environment on genetic composition. J Fish Biol 52:1014–1025

    Article  Google Scholar 

  • Cutts CJ, Metcalfe NB, Taylor AC (1998) Aggression and growth depression in juvenile Atlantic salmon: the consequences of individual variation in standard metabolic rate. J Fish Biol 52:1026–1037

    Article  Google Scholar 

  • David P, Delay B, Berthou P, Jarne P (1995) Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis. Genetics 139:1719–1726

    PubMed  CAS  Google Scholar 

  • Eklund A (1996) The effects of inbreeding on aggression in wild male house mice (Mus domesticus). Behaviour 133:883–901

    Google Scholar 

  • Elliott JM (1994) Quantitative ecology and the brown trout. Oxford University Press, Oxford

    Google Scholar 

  • Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R (1993) (CT)n and (GT)n microsatellites: a new class of genetic markers for Salmo trutta L. (brown trout). Heredity 71:488–496

    PubMed  CAS  Google Scholar 

  • Estoup A, Rousset F, Michalakis Y, Cornuet J-M, Adriamanga M, Guyomard R (1998) Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salmo trutta). Mol Ecol 7:339–353

    Article  PubMed  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hansson B, Westerdahl H, Hasselquist D, Åkesson 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 

  • Holtby LB, Swain DP, Allan GM (1993) Mirror-elicited agonistic behaviour and body morphology as predictors of dominance status in juvenile coho salmon (Oncorhycnhus kisutch). Can J Fish Aquat Sci 50:676–684

    Google Scholar 

  • Huntingford FA, Turner AK (1987) Animal conflict. Chapman and Hall, London

    Google Scholar 

  • Höglund J, Piertney SB, Alatalo R, Lindell J, Lundberg A, Rintamäki PT (2002) Inbreeding and male fitness in a wild population. Proc R Soc Lond B 269:711–715

    Article  Google Scholar 

  • Höjesjö J, Johnsson JI, Bohlin T (2002) Can laboratory studies on dominance predict fitness of young brown trout in the wild? Behav Ecol Sociobiol 52:102–108

    Article  Google Scholar 

  • Lahti K, Laurila A, Enberg K, Piironen J (2001) Variation in aggressive behaviour among populations and migration forms in brown trout (Salmo trutta). Anim Behav 62:935–944

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for mixed models. SAS Institute, Cary, NC

    Google Scholar 

  • Maynard Smith J (1956) Fertility, mating behaviour and sexual selection in Drosophila subobscura. J Genet 54:261–279

    Google Scholar 

  • Meagher S, Penn DJ, Potts WK (2000) Male–male competition magnifies inbreeding depression in wild house mice. Proc Natl Acad Sci U S A 97:3324–3329

    Article  PubMed  CAS  Google Scholar 

  • Metcalfe NB (1998) The interaction between behaviour and physiology in determining the life history patterns in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:93–103

    Article  Google Scholar 

  • Metcalfe NB, Huntingford FA, Graham WD, Thorpe JE (1989) Early social status and the development of life-history strategies in Atlantic salmon. Proc R Soc Lond B 236:7–19

    PubMed  CAS  Google Scholar 

  • Metcalfe NB, Huntingford FA, Thorpe JE, Adams CE (1990) The effects of social status on life history variation in juvenile salmon. Can J Fish Aquat Sci 68:2630–2636

    Google Scholar 

  • Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436

    Article  Google Scholar 

  • Nakano S (1995) Individual differences in resource use, growth and emigration under the influence of a dominance hierarchy in fluvial red-spotted masu salmon in a natural habitat. J Anim Ecol 64:75–84

    Article  Google Scholar 

  • Nielsen JL (1998) Population genetics and the conservation and management of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55(suppl 1):145–152

    Article  Google Scholar 

  • O’Reilly PT, Hamilton LC, McConnell SK, Wright JM (1996) Rapid detection of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fish Aquat Sci 53:2292–2298

    Article  CAS  Google Scholar 

  • Pemberton JM (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615

    Article  PubMed  Google Scholar 

  • Pemberton JM, Coltman DW, Coulson TN, Slate J (1999) Using microsatellites to measure the fitness consequences of inbreeding and outbreeding. In: Goldstein DB, Schlötterer C (eds) Microsatellites. Evolution and applications. Oxford University Press, Oxford, pp 151–164

    Google Scholar 

  • Poteaux C (1995) Interactions génétiques entre formes sauvages et formes domestiques chez la truite commune (Salmo trutta fario L.) Ph.D. thesis, Université Montpellier II, Montpellier

  • Presa P, Guyomard R (1996) Conservation of microsatellites in three species of salmonids. J Fish Biol 49:1326–1329

    Google Scholar 

  • Primmer CR, Aho T, Piironen J, Estoup A, Cornuet J-M, Ranta E (1999) Microsatellite analysis of hatchery stocks and natural populations of Arctic charr, Salvelinus alpinus, from the Nordic region: implications for conservation. Hereditas 130:227–289

    Article  Google Scholar 

  • Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831

    Article  PubMed  CAS  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barrath EM (2001) Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum). Proc R Soc Lond B 268:1055–1061

    Article  CAS  Google Scholar 

  • Ryman N, Ståhl G (1980) Genetic changes in hatchery stocks of brown trout (Salmo trutta). Can J Fish Aquat Sci 37:82–87

    Article  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    Article  CAS  Google Scholar 

  • Scribner KT, Gust JR, Fields RL (1996) Isolation and characterisation of novel salmon microsatellite loci: cross-species amplification and population genetic applications. Can J Fish Aquat Sci 53:833–841

    Article  CAS  Google Scholar 

  • Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. J Evol Biol 15:20–31

    Article  Google Scholar 

  • Slate J, Kruuk LEB, Markshall TC, Pemberton JM, Clutton-Brock TH (2000) Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc R Soc Lond B 267:1657–1662

    Article  CAS  Google Scholar 

  • Slettan AI, Olsaker I, Lie Ø (1995) Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim Genet 26:281–282

    PubMed  CAS  Google Scholar 

  • Tiira K, Laurila A, Peuhkuri N, Piironen J, Ranta E, Primmer CR (2003) Aggressiveness is associated with genetic diversity in landlocked salmon (Salmo salar). Mol Ecol 12:2399–2407

    Article  PubMed  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 

Download references

Acknowledgement

We thank Finnish Game and Fisheries Research for allowing the use of brown trout stocks in this study, and Saimaa Fisheries Research and Aquaculture for excellent working facilities. T. Aho helped in transporting the eggs, and S. Vilhunen assisted in fish maintenance. Special thanks for B. Amos’ aid with calculating the heterozygosity–heterozygosity correlations. J. Höglund, J. Merilä, N. Metcalfe and N. Peuhkuri gave constructive comments on the manuscript. Our research was funded by the Finnish Game and Fisheries Research Institute, the Finnish Ministry of Education (to K.T.) and the Academy of Finland [K.T. (project no. 80705), A.L. (project no. 164206), C.R.P. (project no. 17296), Sami Aikio and E.R. (project no. 162961)]. Fish in this study were handled according to Guidelines for the Use of Animals in Research and according to national legal guidelines.

Author information

Author notes

  1. Anssi Laurila

    Present address: Population Biology/Department of Ecology and Evolution, Evolutionary Biology Centre, University of Uppsala, Norbyvägen 18d, 75236, Uppsala, Sweden

Authors and Affiliations

  1. Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014, Helsinki, Finland

    Katriina Tiira, Anssi Laurila, Sami Aikio & Esa Ranta

  2. Department of Mathematics and Statistics, University of Helsinki, P.O. Box 68, 00014, Helsinki, Finland

    Katja Enberg

  3. Joensuu Game and Fisheries Research, Yliopistonkatu 6, 80100, Joensuu, Finland

    Jorma Piironen

  4. Department of Biology, University of Turku, 20014, Turku, Finland

    Craig R. R. Primmer

Authors
  1. Katriina Tiira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anssi Laurila
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katja Enberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorma Piironen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sami Aikio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Esa Ranta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Craig R. R. Primmer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katriina Tiira.

Additional information

Communicated by C. St. Mary

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tiira, K., Laurila, A., Enberg, K. et al. Do dominants have higher heterozygosity? Social status and genetic variation in brown trout, Salmo trutta . Behav Ecol Sociobiol 59, 657–665 (2006). https://doi.org/10.1007/s00265-005-0094-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-005-0094-8

Keywords

Search

Navigation