Skip to main content
SpringerLink
Log in

Rapid genetic deterioration in captive populations: Causes and conservation implications

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Many species require captive breeding to ensuretheir survival. The eventual aim of suchprograms is usually to reintroduce the speciesinto the wild. Populations in captivitydeteriorate due to inbreeding depression, lossof genetic diversity, accumulation of newdeleterious mutations and genetic adaptationsto captivity that are deleterious in the wild.However, there is little evidence on themagnitude of these problems. We evaluatedchanges in reproductive fitness in populationsof Drosophila maintained under benigncaptive conditions for 50 generations witheffective population sizes of 500 (2replicates), 250 (3), 100 (4), 50 (6) and 25(8). At generation 50, fitness in the benigncaptive conditions was reduced in smallpopulations due to inbreeding depression andincreased in some of the large populations dueto modest genetic adaptation. When thepopulations were moved to `wild' conditions,all 23 populations showed a marked decline(64–86%percnt;) in reproductive fitness compared tocontrols. Reproductive fitness showed acurvilinear relationship with population size,the largest and smallest population sizetreatments being the worst. Genetic analysesindicated that inbreeding depression andgenetic adaptation were responsible for thegenetic deterioration in `wild' fitness.Consequently, genetic deterioration incaptivity is likely to be a major problem whenlong-term captive bred populations ofendangered species are returned to the wild. Aregime involving fragmentation of captivepopulations of endangered species is suggestedto minimize the problems.

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

Similar content being viewed by others

References

  • Allendorf, FW (1993) Delay of adaptation to captive breeding by equalizing family size. Conserv. Biol., 7, 416–419.

    Google Scholar 

  • Arnold SJ (1995) Monitoring quantitative genetic variation and evolution in captive populations. In: Population Management for Survival & Recovery: Analytical Methods and Strategies in Small Population Conservation (eds. Ballou JD, Gilpin M, Foose TJ), pp. 295–317. Columbia University Press, New York.

    Google Scholar 

  • Ballou J, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Population Management for Survival and Recovery: Analytical Methods and Strategies in Small Population Conservation (eds. Ballou J, Gilpin M, Foose T), pp. 76–111. Columbia University Press, New York.

    Google Scholar 

  • Beck BB, Rapaport LG, Stanley Price MR, Wilson AC (1994) Reintroduction of captive-born animals. In: Creative Conservation: Interactive Management of Wild and Captive Animals (eds. Olney PJS Mace GM, Feistner ATC), pp. 265–286. Chapman & Hall, London.

    Google Scholar 

  • Borlase SC, Loebel DA, Frankham R, Nurthen RK, Briscoe DA, Daggard GE (1993) Modeling problems in conservation genetics using captive Drosophila populations: Consequences of equalization of family sizes. Conserv. Biol., 7, 122–131.

    Google Scholar 

  • Bush GL, Neck RW, Kitto GB (1976) Screwworm eradication: Inadvertent selection for noncompetitive ecotypes during mass rearing. Science, 193, 491–493.

    Google Scholar 

  • Caballero A, Toro MA, Lopez-Fanjul C (1991) The response to artificial selection from new mutations in Drosophila melanogaster. Genetics, 128, 89–102.

    Google Scholar 

  • Chilcote MW, Leider SA, Loch JJ (1986) Differential reproductive success of hatchery and wild summer-run steelhead under natural conditions. Trans. Amer. Fisheries Soc., 115, 727–735.

    Google Scholar 

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

    Google Scholar 

  • Cruden D (1949) The computation of inbreeding coefficients in closed populations. J. Hered., 40, 248–251.

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics (Fourth ed.). Harlow, Longman, Harlow, Essex.

    Google Scholar 

  • Fleming IA, Gross MT (1993) Breeding success of hatchery and wild coho salmon (Oncorhynchus kisutch) in competition. Ecol. Applic., 3, 230–245.

    Google Scholar 

  • Fleming IA, Hindar K, Mjolnerod IB, Jonsson B, Balstad T, Lamberg A (2000) Lifetime success and interactions of farm salmon invading a native population. Proc. Roy. Soc. Lond. B, 267, 1517–1523.

    Google Scholar 

  • Frankham R (1995) Genetic management of captive populations for reintroduction. In: Reintroduction Biology of Australian and New Zealand Fauna (ed. Serena M), pp. 31–34. Surrey Beatty & Sons, Chipping Norton, NSW

    Google Scholar 

  • Frankham R, Loebel DA (1992) Modeling problems in conservation genetics using captive Drosophila populations: Rapid genetic adaptation to captivity. Zoo Biol., 11, 333–342.

    Google Scholar 

  • Frankham R, Manning H, Margan SH, Briscoe DA (2000) Does equalisation of family sizes reduce genetic adaptation to captivity? Anim. Conserv., 3, 357–363.

    Google Scholar 

  • Frankham R, Yoo BH, Sheldon BL (1988) Reproductive fitness and artificial selection in animal breeding: Culling on fitness prevents a decline in reproductive fitness in lines of Drosophila melanogaster selected for increased inebriation time. Theor. Appl. Genet., 76, 909–914.

    Google Scholar 

  • Fraser JM (1981) Comparative survival and growth of planted wild, hybrid, and domestic strains of brook trout (Salvelinus fontinalis) in Ontario Lakes. Can. J. Fish. Aquatic Sci., 38, 1372–1384.

    Google Scholar 

  • Gilligan DM (2001) Conservation Genetics and Long Term Survival: Testing Models using Drosophila. Ph.D. thesis, Macquarie University, Sydney, Australia.

    Google Scholar 

  • Gilligan DM, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (1997) Is mutation accumulation a threat to the survival of endangered populations? Conserv. Biol., 11, 1235–1241.

    Google Scholar 

  • Gipps JHW (ed.) (1991) Beyond Captive Breeding: Re-introducing Endangered Mammals into the Wild. Clarendon Press, Oxford.

    Google Scholar 

  • Haymer DS, Hartl DL (1982) The experimental assessment of fitness in Drosophila. I. Comparative measures of competitive reproductive success. Genetics, 102, 455–466.

    Google Scholar 

  • Haymer DS, Hartl DL (1983) The experimental assessment of fitness in Drosophila. II. Comparison of competitive and noncompetitive measures. Genetics, 104, 343–352.

    Google Scholar 

  • Heschel MS, Paige KN (1995) Inbreeding depression, environmental stress, and population size variation in scarlet gilia (Ipomopsis aggregata). Conserv. Biol., 9, 126–133.

    Google Scholar 

  • Hill WG (1982) Predictions of response to artificial selection from new mutations. Genet. Res., 40, 255–278.

    Google Scholar 

  • Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can. J. Fish. Aquatic Sci., 48, 945–957.

    Google Scholar 

  • Hoffmann AA, Parsons PA (1991) Evolutionary Genetics and Environmental Stress. Oxford University Press, Oxford.

    Google Scholar 

  • Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Nat. Acad. Sci. USA, 96, 5083–5088.

    Google Scholar 

  • IUCN (1987) IUCN Policy Statement on Translocation of Living Organisms: Introductions, Reintroductions and Restocking. IUCN Council, Gland, Switzerland.

    Google Scholar 

  • IUCN (1996) 1996 IUCN Red List of Threatened Animals. IUCN Council, Gland, Switzerland.

    Google Scholar 

  • Jungen H, Hartl DL (1979) Average fitness of populations of Drosophila melanogaster as estimated using compound-autosome strains. Evolution, 33, 359–370.

    Google Scholar 

  • Kimura M (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge, England.

    Google Scholar 

  • Kimura M, Crow JF (1963) On the maximum avoidance of inbreeding. Genet. Res., 4, 399–415.

    Google Scholar 

  • Lachance S, Magnan P (1990) Performance of domestic, hybrid, and wild strains of brook trout, Salvelinus fontinalis, after stocking: The impact of intra-and interspecific competition. Can. J. Fish. Aquatic Sci., 47, 2278–2284.

    Google Scholar 

  • Lacy RC (1997) Importance of genetic variation in the viability of mammalian populations. J. Mammal., 78, 320–335.

    Google Scholar 

  • Lande R (1995) Mutation and conservation. Conserv. Biol., 9, 782–791.

    Google Scholar 

  • Latter BDH, Mulley JC (1995) Genetic adaptation to captivity and inbreeding depression in small laboratory populations of Drosophila melanogaster. Genetics, 139, 255–266.

    Google Scholar 

  • Leary RF, Allendorf FW, Knudsen KL (1993) Null allele heterozygosity at two lactate dehydrogenase loci in rainbow trout are associated with decreased developmental stability. Genetica, 89, 3–13.

    Google Scholar 

  • Leopold AS (1944) The nature of heritable wildness in turkeys. Condor, 46, 133–197.

    Google Scholar 

  • Lynch M, Conery J, Burger R (1995) Mutational meltdowns in sexual populations. Evolution, 49, 1067–1080.

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA.

    Google Scholar 

  • Margan SH, Nurthen RK, Montgomery ME, Woodworth LM, Briscoe DA Frankham R (1998) Single large or several small? Population fragmentation in the captive management of endangered species. Zoo Biol., 17, 467–480.

    Google Scholar 

  • Miller PS (1994) Is inbreeding depression more severe in a stressful environment? Zoo Biol., 13, 195–208.

    Google Scholar 

  • Montgomery ME, Ballou JD, Nurthen RK, Briscoe DA, Frankham R (1997) Minimizing kinship in captive breeding programs. Zoo Biol., 16, 377–389.

    Google Scholar 

  • Montgomery ME, Woodworth LM, Nurthen RK, Gilligan DM, Briscoe DA Frankham R (2000) Relationships between population size and loss of genetic diversity: Comparisons of experimental results with theoretical predictions. Conserv. Genet., 1, 33–43.

    Google Scholar 

  • Myers D, Sabath MD (1980) Genetic and phenotypic variability, genetic variance, and the success of establishment of insect introductions for the biological control of weeds. Proc. V Int. Sym. on Biological Control of Weeds, pp. 91–102. Brisbane, Australia.

  • Nunney L (2001) Managing captive populations for release: A population genetic perspective. In: Quality Control of Natural Enemies used in Biological Pest Control: Theoretical Background and Development of Testing Procedures (ed. van Lenteren JC). Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Ralls K, Ballou JD (1983) Extinction: Lessons from zoos. In: Genetics and Conservation: A Reference for Managing Wild Animal and Plant Populations (eds. Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas L), pp. 164–184. Benjamin/ Cummings, Menlo Park, CA.

    Google Scholar 

  • Ralls K, Ballou J (eds.) (1986) Proceedings of the workshop on genetic management of captive populations. Zoo Biol., 5, 81–238.

    Google Scholar 

  • Reisenbichler RR, Rubin SP (1999) Genetic changes from artificial propagation of Pacific salmon affect the productivity and viability of supplemented populations. ICES J. Mar. Sci., 56, 459–466.

    Google Scholar 

  • Robertson A (1960) A theory of limits in artificial selection. Proc. Roy. Soc. Lond. B, 153, 234–249.

    Google Scholar 

  • Robertson A (1964) The effect of non-random mating within inbred lines on the rate of inbreeding. Genet. Res., 5, 164–167.

    Google Scholar 

  • Rumball W, Franklin IR, Frankham R, Sheldon BL (1994) Decline in heterozygosity under full-sib and double first-cousin inbreeding in Drosophila melanogaster. Genetics, 136, 1039–1049.

    Google Scholar 

  • Shabalina SA, Yampolsky LY, Kondrashov AS (1997) Rapid decline in fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc. Nat. Acad. Sci. USA, 94, 13034–13039.

    Google Scholar 

  • Soulé ME, Gilpin M, Conway W, Foose T (1986) The millennium ark: How long a voyage, how many staterooms, how many passengers? Zoo Biol., 5, 101–113.

    Google Scholar 

  • Stanley Price M, Gordon I (1989) How to go wild. New Scient., 124(1688), 40–42.

    Google Scholar 

  • Tudge C (1995) Captive audiences for future conservation. New Scient., 145(1962), 51–52.

    Google Scholar 

  • Weber KE, Diggins LT (1990) Increased selection response in larger populations. II. Selection for ethanol vapor resistance in Drosophila melanogaster, at two population sizes. Genetics, 125, 585–597.

    Google Scholar 

  • Wilson AC, Stanley Price MR (1994) Reintroduction as a reason for captive breeding. In: Creative Conservation: Interactive Management of Wild and Captive Animals (eds. Olney PJS, Mace GM, Feistner ATC), pp. 243–264. Chapman & Hall, London.

    Google Scholar 

  • Woodworth LM (1996) Population Size in Captive Breeding Programs. Ph.D. thesis, Macquarie University, Sydney, Australia.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Centre for Biodiversity and Bioresources, Department of Biological Science, Macquarie University, NSW, 2109, Australia

    Lynn M. Woodworth, Margaret E. Montgomery, David A. Briscoe & Richard Frankham

Authors
  1. Lynn M. Woodworth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margaret E. Montgomery
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David A. Briscoe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard Frankham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard Frankham.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Woodworth, L.M., Montgomery, M.E., Briscoe, D.A. et al. Rapid genetic deterioration in captive populations: Causes and conservation implications. Conservation Genetics 3, 277–288 (2002). https://doi.org/10.1023/A:1019954801089

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1019954801089

Search

Navigation