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Inbreeding, inbreeding depression and extinction

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Abstract

Inbreeding is unavoidable in small, isolated populations and can cause substantial fitness reductions compared to outbred populations. This loss of fitness has been predicted to elevate extinction risk giving it substantial conservation significance. Inbreeding may result in reduced fitness for two reasons: an increased expression of deleterious recessive alleles (partial dominance hypothesis) or the loss of favourable heterozygote combinations (overdominance hypothesis). Because both these sources of inbreeding depression are dependent upon dominance variance, inbreeding depression is predicted to be greater in life history traits than in morphological traits. In this study we used replicate inbred and control lines of Drosophila simulans to address three questions:1) is inbreeding depression greater in life history than morphological traits? 2) which of the two hypotheses is the major underlying cause of inbreeding depression? 3) does inbreeding elevate population extinction risk? We found that inbreeding depression was significantly greater in life history traits compared to morphological traits, but were unable to find unequivocal support for either the overdominance or partial dominance hypotheses as the genetic basis of inbreeding depression. As predicted, inbred lines had a significantly greater extinction risk.

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References

  • Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J Hered 88:169–178

    PubMed  CAS  Google Scholar 

  • Barrett SCH, Charlesworth D (1991) Effects of a change in the level of inbreeding on the genetic load. Nature 352:522–524

    Article  PubMed  CAS  Google Scholar 

  • Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J Evol Biol 13:502–514

    Article  Google Scholar 

  • Bijlsma R, Bundgaard J, Van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J Evol Biol 12:1125–1137

    Article  Google Scholar 

  • Byers DL, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340

    Article  PubMed  CAS  Google Scholar 

  • Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  • Crnokrak P, Roff DA (1995) Dominance variance––associations with selection and fitness. Heredity 75:530–540

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Demerec M (1994) Biology of Drosophila. Cold Spring Harbour Laboratory Press, New York

    Google Scholar 

  • DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288–1292

    Article  Google Scholar 

  • Dudash MR, Carr DE (1998) Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature 393:682–684

    Article  CAS  Google Scholar 

  • Drewniak M, Radwan J (2001) Inbreeding depression for size but not for symmetry in Drosophila melanogaster. Hereditas 134:85–89

    Article  PubMed  Google Scholar 

  • Ellmer M, Andersson S (2004) Inbreeding depression in Nigella degenii (Ranunculaceae): fitness components compared with morphological and phenological characters. Int J Plant Sci 165:1055–1061

    Article  Google Scholar 

  • Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Longman, New York

    Google Scholar 

  • Fowler K, Whitlock MC (1999) The distribution of phenotypic variance with inbreeding. Evolution 53:1143–1156

    Article  Google Scholar 

  • Frankham R (1995a) Conservation genetics. Ann Rev Genet 29:305–327

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995b) Inbreeding and extinction––a threshold effect. Cons Biol 9:792–799

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

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

    Google Scholar 

  • Gilchrist AS, Partridge L (2001) The contrasting genetic architecture of wing size and shape in Drosophila melanogaster. Heredity 86:144–152

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (1994) Purging inbreeding depression and the probability of extinction––full-sib mating. Heredity 73:363–372

    Article  PubMed  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford, University Press, Oxford, UK

    Google Scholar 

  • Hughes KA (1995) The inbreeding decline and average dominance of genes affecting male life-history characters in Drosophila melanogaster. Genet Res 65:41–52

    Article  PubMed  CAS  Google Scholar 

  • Karkkainen K, Kuittinen H, van Treuren R, Vogl C, Oikarinen S, Savolainen O (1999) Genetic basis of inbreeding depression in Arabis petraea. Evolution 53:1354–1365

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kosuda K (1980) The effect of inbreeding on viability in Drosophila simulans. Jpn J Genet 55:307–310

    Article  Google Scholar 

  • Kristensen TN, Dahlgaard J, Loeschcke V (2003) Effects of inbreeding and environmental stress on fitness––using Drosophila buzzatii as a model organism. Conserv Genet 4:453–465

    Article  Google Scholar 

  • Kristensen TN, Sorensen AC (2005) Inbreeding––lessons from animal breeding, evolutionary biology and conservation genetics. Animal Sci 80:121–133

    Google Scholar 

  • Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution 39:24–40

    Article  Google Scholar 

  • Lessels CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Li ZK, Luo LJ, Mei HW, Wang DL, Shu QY, Tabien R, Zhong DB, Ying CS, Stansel JW, Khush GS, Paterson AH (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158:1737–1753

    PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland, Massachusetts

    Google Scholar 

  • Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354–362

    Article  Google Scholar 

  • Pray LA, Goodnight CJ (1995) Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49:176–188

    Article  Google Scholar 

  • Radwan J (2003) Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90:371–376

    Article  PubMed  CAS  Google Scholar 

  • Ralls K, Ballou JD, Templeton AR (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Cons Biol 2:185–193

    Article  Google Scholar 

  • Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3:301–307

    Article  CAS  Google Scholar 

  • Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4:405–410

    Article  CAS  Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman & Hall, London

    Google Scholar 

  • Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81:28–37

    Article  Google Scholar 

  • Roff DA (2002) Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution 56:768–775

    PubMed  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 

  • Saccheri I, Wilson IJ, Nichols RA, Bruford MW Brakefield PM (1999) Inbreeding of bottlenecked butterfly populations: estimation using the likelihood of changes in marker allele frequencies. Genetics 151:1053–1063

    PubMed  CAS  Google Scholar 

  • Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50:2000–2013

    Article  Google Scholar 

  • Swindell WR, Bouzat JL (2006a) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762–767

    PubMed  Google Scholar 

  • Swindell WR, Bouzat JL (2006b) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19:1257–1264

    Article  PubMed  CAS  Google Scholar 

  • Tantawy AO (1957) Genetic variance of random-inbred lines of Drosophila melanogaster in relation to coefficients of inbreeding. Genetics 42:121–136

    PubMed  CAS  Google Scholar 

  • Tantawy AO, Reeve ECR (1956) Studies in quantitative inheritance. IX. The effects of inbreeding at different rates in Drosophila melanogaster. Z Ind Abst Vererb 87:648–667

    Article  CAS  Google Scholar 

  • Templeton AR, Read B (1984) Factors eliminating inbreeding depression in a captive herd of spekes gazelle (Gazella spekei). Zoo Biol 3:177–199

    Article  Google Scholar 

  • Whitlock MC, Fowler K (1996) The distribution among populations in phenotypic variance with inbreeding. Evolution 50:1919–1926

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Ary Hoffmann and Jennifer Shirriffs for kindly providing the flies that allowed us to conduct this study, Michelle Taylor for help with rearing the stock populations, the European Social Fund and NERC for funding, and especially François Balloux and an anonymous referee for insightful comments that greatly improved the manuscript.

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Authors and Affiliations

  1. Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Treliever Road, Tremough, Penryn, Cornwall, TR10 9EZ, UK

    Lucy I. Wright, Tom Tregenza & David J. Hosken

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  1. Lucy I. Wright
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  2. Tom Tregenza
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  3. David J. Hosken
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Correspondence to David J. Hosken.

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Wright, L.I., Tregenza, T. & Hosken, D.J. Inbreeding, inbreeding depression and extinction. Conserv Genet 9, 833–843 (2008). https://doi.org/10.1007/s10592-007-9405-0

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  • DOI: https://doi.org/10.1007/s10592-007-9405-0

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