Skip to main content Accessibility help

Inbreeding – lessons from animal breeding, evolutionary biology and conservation genetics

  • T. N. Kristensen (a1) (a2) and A. C. Sørensen (a1) (a3)


Abstract Increased rates of inbreeding are one side effect of breeding programmes designed to give genetic progress for traits of economic importance in livestock. Inbreeding leads to inbreeding depression for traits showing dominance, and will ultimately lead to a decrease in genetic variance within populations. Here we review theoretical and experimental literature from animal breeding, evolutionary biology and conservation genetics on the consequences of inbreeding in terms of trait means and genetic and environmental variance components. The genetic background for these effects is presented and the experimental literature interpreted in relation to them. Furthermore, purging of deleterious alleles and the variable nature of effects of inbreeding on populations are discussed. Based on the literature, we conclude that inbreeding in animal breeding must be controlled very efficiently to maintain long-term sustainable livestock production in the future. The tools to do this efficiently exist, and much can be learnt on inbreeding from the literature in fields only distantly related to animal breeding.


Corresponding author

Corresponding author. E-mail:


Hide All
Abplanalp, H. 1990. Inbreeding. In Poultry breeding and genetics (ed. Crawford, R.D.), pp. 955984. Elsevier, Amsterdam.
Andersen, B.B., Jensen, B., Nielsen, A., Christensen, L. G. and Liboriussen, T. 2003. Rød Dansk Malkerace – avlsmæssigt og kulturhistorisk belyst. Report no. 50 in animal husbandry from the Danish Institute of Agricultural Sciences.
Anderson, V.L. and Kempthorne, O. 1954. A model for the study of quantitative inheritance. Genetics 9: 883898.
Ballou, J.D. 1997. Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. Journal of Heredity 8: 169178.
Belonsky, G.M. and Kennedy, B.W. 1988. Selection on individual phenotype and best linear unbiased predictor of breeding value in a closed swine herd. Journal of Animal Science 66: 11241131.
Bijlsma, R., Bundgaard, J. and Boerema, A.C. 2000. Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila. Journal of Evolutionary Biology 3: 502514.
Bijlsma, R., Bundgaard, J. and Van Putten, W.F. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology 12: 11251137.
Bohren, B.B., Hill, W.G. and Robertson, A. 1966. Some observations on asymmetrical correlated responses to selection. Genetical Research 7: 4457.
Briskie, J.V. and Mackintosh, M. 2004. Hatching failure increases with severity of population bottlenecks in birds. Proceedings of the National Academy of Sciences of the United States of America 101: 558561.
Bruce, A.B. 1910. The Mendelian theory of heredity and the augmentation of vigor. Science 32: 627628.
Bryant, E.H., McCommas, S.A. and Combs, L.M. 1986. The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114: 11911211.
Bryant, E.H. and Meffert, L. M. 1988. Effect of an experimental bottleneck on morphological integration in the housefly. Evolution 42: 698707.
Buri, P. 1956. Gene frequency in small populations of mutant Drosophila. Evolution 10: 367402.
Charlesworth, B. 1998. The effect of synergistic epistasis on the inbreeding load. Genetical Research 71: 8589.
Charlesworth, B. and Charlesworth, D. 1999. The genetic basis of inbreeding depression. Genetical Research 74: 329340.
Charlesworth, D. and Charlesworth, B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237268.
Christensen, L. G. and Pedersen, J. 1988. [Crossbreeding of dairy cattle.] Report no. 650 from the National Institute of Animal Science, Denmark, Copenhagen.
Clayton, G.A., Morris, J.A. and Robertson, A. 1957. An experimental check on quantitative genetical theory. I. Short-term responses to selection. Journal of Genetics 55: 131151.
Cockerham, C.C. 1984. Additive by additive variance with inbreeding and linkage. Genetics 108: 487500.
Cockerham, C.C. and Weir, B.S. 1973. Descent measures for two loci with some applications. Theoretical Population Biology 4: 300330.
Cockerham, C.C. and Weir, B.S. 1983. Variance of actual inbreeding. Theoretical Population Biology 23: 85109.
Cockerham, C.C. and Weir, B.S. 1984. Covariances of relatives stemming from a population undergoing mixed self and random mating. Biometrics 40: 157164.
Crnokrak, P. and Barrett, S.C.H. 2002. Purging the genetic load: a review of the experimental evidence. Evolution 56: 23472358.
Crnokrak, P. and Roff, D.A. 1999. Inbreeding depression in the wild. Heredity 83: 260270.
Crow, J.F. 1993. Mutation, mean fitness, and genetic load. In Oxford surveys in evolutionary biology (ed. Futuyma, D. and Antonovics, J.), pp. 342. Oxford University Press, NY.
Crow, J.F. and Kimura, M. 1970. An introduction to population genetics theory. Harper and Row, NY.
Darwin, C. 1868. The variation of animals and plants under domestication. John Murray, London.
Darwin, C. 1876. The effects of cross and self-fertilization in the vegetable kingdom. Appleton, NY.
Davenport, C.B. 1908. Degeneration, albinism, and inbreeding. Science 28: 454455.
Day, S.B., Bryant, E.H. and Meffert, L.M. 2003. The infuence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57: 13141324.
DeRose, M.A. and Roff, D.A. 1999. A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53: 12881292.
Dudash, M.R. 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: 11291139.
Ehiobu, N.G., Goddard, M.E. and Taylor, J.F. 1989. Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theoretical and Applied Genetics 77: 123127.
Ellegren, H., Hartman, G., Johansson, M. and Andersson, L. 1993. Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proceedings of the National Academy of Sciences of the United States of America 90: 81508153.
Falconer, D.S. and Mackay, T.F.C. 1996. Introduction to quantitative genetics. Longman, Harlow.
Fernández, A., Toro, M.A. and López-Fanjul, C. 1995. The effect of inbreeding on the redistribution of genetic variance of fecundity and viability in Tribolium castaneum. Heredity 75: 376381.
Fowler, K. and Whitlock, M.C. 1999a. The distribution of phenotypic variance with inbreeding. Evolution 53: 11431156.
Fowler, K. and Whitlock, M.C. 1999b. The variance in inbreeding depression and the recovery of fitness in bottlenecked populations. Proceedings of the Royal Society of London, series B 266: 20612066.
Frankel, O.H. and Soulé, M.E. 1981. Conservation and evolution. Cambridge University Press, Cambridge.
Frankham, R. 1999. Resolving conceptual issues in conservation genetics: the roles of laboratory species and meta-analysis. Hereditas 130: 195201.
Frankham, R., Ballou, J.D. and Briscoe, D.A. 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge.
Frankham, R., Gilligan, D.M., Morris, D. and Briscoe, D.A. 2001. Inbreeding and extinction: effects of purging. Conservation Genetics 2: 279285.
Franklin, I.R. 1980. Evolutionary change in small populations. In Conservation biology: an evolutionary-ecological perspective (ed. Soulé, M.E. and Wilcox, B.A.), pp. 135150. Sinauer, Sunderland, MA.
Franklin, I.R. and Frankham, R. 1998. How large must populations be to retain evolutionary potential? Animal Conservation 1: 6970.
Fu, Y.-B., Namkoong, G. and Carlson, J.E. 1998. Comparison of breeding strategies for purging inbreeding depression via simulation. Conservation Biology 12: 856864.
García, N., López-Fanjul, C. and García-Dorado, A. 1994. The genetics of viability in Drosophila melanogaster: effects of inbreeding and artificial selection. Evolution 48: 12771285.
Gething, M.-J. and Sambrook, J. 1992. Protein folding in the cell. Nature 355: 3345.
Good, R.L. and Hallauer, A.R. 1977. Inbreeding depression in maize by selfing and self-sibbing. Crop Science 17: 935940.
Goodnight, C.J. 1987. On the effect of founder events on epistatic genetic variance. Evolution 41: 8091.
Goodnight, C.J. 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441454.
Hallauer, A.R. and Sears, J.H. 1973. Changes in quantitative traits associated with inbreeding in a synthetic variety of maize. Crop Science 13: 327330.
Hedrick, P.W. 1994. Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73: 363372.
Hedrick, P.W. and Kalinowski, S.T. 2000. Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics 31: 139162.
Hill, W.G. and Robertson, A. 1966. The effects of linkage on limits of artificial selection. Genetical Research 8: 269294.
Hoelzel, A.R., Halley, J., O'Brien, S.J., Campagna, C., Arnbom, T., Le Boeuf, B., Ralls, K. and Dover, G.A. 1993. Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. Journal of Heredity 84: 443449.
Hoeschele, I. 1991. Additive and nonadditive genetic variance in female fertility of Holsteins. Journal of Dairy Science 74: 17431752.
Jones, D.F. 1917. Dominance of linked factors as a means of accounting for heterosis. Genetics 2: 466479.
Joron, M. and Brakefield, P.M. 2003. Captivity masks inbreeding effects on male mating success in butterflies. Nature 424: 191194.
Karkkainen, K., Kuittinen, H., Treuren, R. van Vogl, C., Oikarinen, S. and Savolainen, O. 1999. Genetic basis of inbreeding depression in Arabis petraea. Evolution 53: 13541365.
Keeble, F. and Pellew, C. 1910. The mode of inheritance of stature and of time of flowering in peas Pisum sativum. Journal of Genetics 1: 869876.
Keller, L.F. and Waller, D.M. 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17: 230241.
Kolmodin, R., Strandberg, E., Jorjani, H. and Danell, B. 2003. Selection in the presence of a genotype by environment interaction: response in environmental sensitivity. Animal Science 76: 375385.
Kristensen, T.N., Dahlgaard, J. and Loeschcke, V. 2002. Inbreeding affects Hsp 70 expression in two species of Drosophila even at benign temperatures. Evolutionary Ecology Research 4: 12091216.
Kristensen, T.N., Dahlgaard, J. and Loeschcke, V. 2003. Effects of inbreeding and environmental stress on fitness-using Drosophila buzzatii as a model organism. Conservation Genetics 4: 453465.
Kristensen, T.N., Sørensen, A.C., Sorensen, D., Pedersen, K.S., Sørensen, J.G. and Loeschcke, V. 2005. A test of quantitative genetic theory using Drosophila – effects of inbreeding and rate of inbreeding on heritabilities and variance components. Journal of Evolutionary Biology In press.
Laikre, L., Ryman, N. and Thompson, E.A. 1993. Hereditary blindness in a captive wolf (Canis lupus) population. Conservation Biology 7: 592601.
Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33: 402416.
Lande, R. 1995. Mutation and conservation. Conservation Biology 9: 782791.
Latter, B.D.H., Mulley, J.C., Reid, D. and Pascoe, L. 1995. Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster. Genetics 139: 287297.
Latter, R. and Robertson, A. 1962. The effects of inbreeding and artificial selection on reproductive fitness. Genetical Research 3: 110138.
Lerner, I.M. 1954. Genetic homeostasis. Oliver and Boyd, Edinburgh.
Lewontin, R.C. 1974. The analysis of variance and the analysis of causes. American Journal of Human Genetics 26: 400411.
Li, Z.K., Luo, L.J., Mei, H.W., Wang, D.L., Shu, Q.Y., Tabien, R., Zhong, D.B., Ying, C.S., Stansel, J.W., Khush, G.S. and Paterson, A.H. 2001. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice.I. Biomass and grain yield. Genetics 158: 17371753.
López-Fanjul, C., Fernández, A. and Toro, M.A. 1999. The role of epistasis in the increase in the additive genetic variance after population bottlenecks. Genetical Research 73: 4559.
López-Fanjul, C., Fernández, A. and Toro, M.A. 2000. Epistasis and the conversion of non-additive genetic variance at population bottlenecks. Theoretical Population Biology 58: 4959.
López-Fanjul, C., Fernández, A. and Toro, M.A. 2002. The effect of epistasis on the excess of the additive and nonadditive variances after population bottlenecks. Evolution 56: 865876.
López-Fanjul, C., Guerra, J. and García, A. 1989. Changes in the distribution of the genetic variance of a quantitative trait in small populations of Drosophila melanogaster. Genetics, Selection, Evolution 21: 159168.
López-Fanjul, C. and Villaverde, A. 1989. Inbreeding increases genetic variance for viability in Drosophila melanogaster. Evolution 43: 18001804.
Lynch, M. 1988. Design and analysis of experiments on random drift and inbreeding depression. Genetics 120: 791807.
Lynch, M. and Walsh, B. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MA.
Madsen, T., Shine, R., Olsson, M. and Wittzell, H. 1999. Restoration of an inbred adder population. Nature 402: 3435.
Malécot, P. 1948. Les mathématiques de l'hérédité. Masson, Paris.
Man, W.Y.N., James, J.W. and Nicholas, F.W. 2002. Effect of inbreeding contribution from particular ancestors: a preliminary analysis of first lactation milk yields from Holstein Friesians in Australia. Proceedings of the seventh world congress on genetics applied to livestock production,Montpellier, CD-ROM communication[23–01].
Meagher, S., Penn, D.J. and Potts, W.K. 2000. Male-male competition magnifies inbreeding depression in wild house mice. Proceedings of the National Academy of Sciences of the United States of America 97: 33243329.
Meuwissen, T.H.E. 1997. Maximizing the response of selection with a predefined rate of inbreeding. Journal of Animal Science 75: 934940.
Meuwissen, T.H.E. and Woolliams, J.A. 1994. Effective sizes of livestock populations to prevent a decline in fitness. Theoretical and Applied Genetics 89: 10191026.
Miglior, F., Burnside, E.B. and Hohenboken, W.D. 1994. Heterogeneity among families of Holstein cattle in inbreeding depression for production traits. Proceedings of the fifth world congress on genetics applied to livestock production, Guelph, vol. 18, pp. 479482.
Miglior, F., Burnside, E.B. and Kennedy, B.W. 1995. Production traits of Holstein cattle: estimation of nonadditive genetic variance components and inbreeding depression. Journal of Dairy Science 78: 11741180.
Misztal, I., Lawlor, T.J. and Gengler, N. 1997. Relationships among estimates of inbreeding depression, dominance and additive variance for linear traits in Holsteins. Genetics, Selection, Evolution 29: 319326.
Mitton, J.B. 1993. Enzyme heterozygosity, metabolism, and developmental stability. Genetica 89: 4765.
Nicholas, F.W. and Smith, C. 1983. Increased rates of genetic change in dairy cattle by embryo transfer and splitting. Animal Production 36: 341353.
Pedersen, K.S., Kristensen, T.N. and Loeschcke, V. 2005. Effects of inbreeding and rate of inbreeding in Drosophila melanogaster – Hsp70 expression and fitness. Journal of Evolutionary Biology In press.
Phillips, P.C., Whitlock, M.C. and Fowler, K. 2001. Inbreeding changes the shape of the genetic covariance matrix in Drosophila melanogaster. Genetics 158: 11371145.
Pirchner, F. 1985. Genetic structure of populations.I. Closed populations or matings among related individuals. In General and quantitative genetics (ed. Chapman, A.B.), pp. 227250. Elsevier, Amsterdam.
Pusey, A. and Wolf, M. 1996. Inbreeding avoidance in animals. Trends in Ecology and Evolution 11: 201206.
Queitsch, C., Sangster, T.A. and Lindquist, S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417: 618624.
Ralls, K. and Ballou, J. 1983. Extinction: lessons from zoos. In Genetics and conservation: a reference for managing wild animal and plant populations (ed. Schonewald-Cox, S.M. Chambers, B. MacBryde, B. and Thomas, L.), pp. 164184. Benjamin/Cummings, Menlo Park, CA.
Ralls, K., Ballou, J.D. and Templeton, A. 1988. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology 2: 185193.
Reed, D.H., Briscoe, D.A. and Frankham, R. 2002. Inbreeding and extinction: the effect of environmental stress and lineage. Conservation Genetics 3: 301307.
Reed, D.H. and Bryant, E.H. 2000. Experimental tests of minimum viable population size. Animal Conservation 3: 714.
Reed, D.H., Lowe, E.H., Briscoe, D.A. and Frankham, R. 2003. Inbreeding and extinction: effects of rate of inbreeding. Conservation Genetics 4: 405410.
Robertson, A. 1952. The effect of inbreeding on the variation due to recessive genes. Genetics 37: 189207.
Rutherford, S.L. and Lindquist, S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336342.
Rye, M. and Mao, I.L. 1998. Nonadditive genetic effects and inbreeding depression for body weight in Atlantic salmon (Salmo salar L.). Livestock Production Science 57: 1522.
Sánchez, L., Bijma, P. and Woolliams, J.A. 2003. Minimizing inbreeding by managing genetic contributions across generations. Genetics 164: 15891595.
Smith, L.A., Cassell, B.G. and Pearson, R.E. 1998. The effects of inbreeding on the lifetime performance of dairy cattle. Journal of Dairy Science 81: 27292737.
Sonesson, A.K., Grundy, B., Woolliams, J.A. and Meuwissen, T.H.E. 2000. Selection with control of inbreeding in populations with overlapping generations: a comparison of methods. Animal Science 70: 18.
Stearns, S.C., Kaiser, M. and Kawecki, T.J. 1995. The differential genetic and environmental canalization of fitness components in Drosophila melanogaster. Journal of Evolutionary Biology 8: 539557.
Sørensen, J.G., Kristensen, T.N. and Loeschcke, V. 2003. The evolutionary and ecological role of heat shock proteins. Ecology Letters 6: 10251037.
Templeton, A.R. and Read, B. 1984. Factors eliminating inbreeding depression in a captive herd of Speke's gazelle (Gazella spekei). spekei Zoo Biology 3: 177199.
Templeton, A.R. and Read, B. 1994. Inbreeding: one word, several meanings, much confusion. In Conservation genetics (ed. Loeschcke, V., Tomiuk, J. and Jain, S.K.), pp. 91105. Birkhäuser, Basel.
Vermeulen, C.J. and Bijlsma, R. 2004. Characterization of conditionally expressed mutants affecting age-specific survival in inbred lines of Drosophila melanogaster: Lethal conditions and temperature sensitive periods. Genetics 167: 12411248.
Verrier, É., Colleau, J.J. and Foulley, J.-L. 1993. Long-term effects of selection based on the animal model BLUP in a finite population. Theoretical and Applied Genetics 87: 446454.
Visscher, P.M., Smith, D., Hall, S.J.G. and Williams, J.L. 2001. A viable herd of genetically uniform cattle. Nature 409: 303.
Waddington, C.H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563565.
Waller, D.M. 1993. The statics and dynamics of mating systems. In The natural history of inbreeding and outbreeding: theoretical and emperical perspectives (ed. Thornhill, N.W.), pp.97117. University of Chicago Press, Chicago.
Walsh, B. and Lynch, M. 1998. Evolution and selection of quantitative traits.
Wang, J., Caballero, A., Keightley, P.D. and Hill, W.G. 1998. Bottleneck effect on genetic variance: a theoretical investigation of the role of dominance. Genetics 150: 435447.
Wang, S., Hard, J.J. and Utter, F. 2002. Salmonid inbreeding: a review. Reviews in Fish Biology and Fisheries 11: 301319.
Wang, J., Hill, W.G., Charlesworth, D. and Charlesworth, B. 1999. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genetical Research 74: 165178.
Weir, B.S., Avery, P.J. and Hill, W.G. 1980. Effect of mating structure on variation in inbreeding. Theoretical Population Biology 18: 396429.
Weir, B.S. and Cockerham, C.C. 1969. Group inbreeding with two linked loci. Genetics 63: 711742.
White, J.M. 1972. Inbreeding effects upon growth and maternal ability in laboratory mice. Genetics 70: 307317.
Whitlock, M.C. and Fowler, K. 1996. The distribution among populations in phenotypic variance with inbreeding. Evolution 50: 19191926.
Whitlock, M.C. and Fowler, K. 1999. The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152: 345353.
Whitlock, M.C., Phillips, P.C. and Fowler, K. 2002. Persistence of changes in the genetic covariance matrix after a bottleneck. Evolution 56: 19681975.
Whitlock, M.C., Phillips, P.C. and Wade, M.J. 1993. Gene interaction affects the additive genetic variance in subdivided populations with migration and extinction. Evolution 47: 17581769.
Wiener, G., Lee, G.J. and Woolliams, J.A. 1992a. Effects of rapid inbreeding and of crossing of inbred lines on the body weight growth of sheep. Animal Production 55: 8999.
Wiener, G., Lee, G.J. and Woolliams, J.A. 1992b. Effects of rapid inbreeding and of crossing of inbred lines on the growth of linear body dimensions of sheep. Animal Production 55: 101114.
Wiener, G., Lee, G.J. and Woolliams, J.A. 1992c. Effects of rapid inbreeding and of crossing of inbred lines on conception rate, prolificacy and ewe survival in sheep. Animal Production 55: 115121.
Wiener, G., Lee, G.J. and Woolliams, J.A. 1994. Consequences of inbreeding for financial returns from sheep. Animal Production 59: 245249.
Willis, J.H. and Orr, H.A. 1993. Increased heritable variation following population bottlenecks: the role of dominance. Evolution 47: 949957.
Woolliams, J.A. and Bijma, P. 2000. Predicting rates of inbreeding in populations undergoing selection. Genetics 154: 18511864.
Wray, N.R. and Goddard, M.E. 1994. Increasing long-term response to selection. Genetics, Selection, Evolution 26: 431451.
Wright, S. 1951. The genetical structure of populations. Annals of Eugenics 15: 323354.



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed