Skip to main content

Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species

Abstract

Captive breeding has become an important tool in species conservation programmes. Current management strategies for ex situ populations are based on theoretical models, which have mainly been tested in model species or assessed using studbook data. During recent years an increasing number of molecular genetic studies have been published on captive populations of several endangered species. However, a comprehensive analysis of these studies is still outstanding. Here, we present a review of the published literature on ex situ conservation genetics with a focus on molecular studies. We analysed 188 publications which either presented empirical studies using molecular markers (105), studbook analyses (26), theoretical work (38), or tested the genetic effects of management strategies using model species (19). The results show that inbreeding can be minimized by a thorough management of captive populations. There seems to be a minimum number of founders (15) and a minimum size of a captive population (100) necessary in order to minimize a loss of genetic diversity. Optimally, the founders should be unrelated and new founders should be integrated into the captive population successively. We recommend that genetic analyses should generally precede and accompany ex situ conservation projects in order to avoid inbreeding and outbreeding depression. Furthermore, many of the published studies do not provide all the relevant parameters (founder size, captive population size, Ho, He, inbreeding coefficients). We, therefore, propose that a general standard for the presentation of genetic studies should be established, which would allow integration of the data into a global database.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alcaide M, Negro JJ, Serrano D et al (2010) Captive breeding and reintroduction of the lesser kestrel Falco naumanni: a genetic analysis using microsatellites. Conserv Genet 11:331–338

    Article  Google Scholar 

  2. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, Oxford, UK

    Google Scholar 

  3. Ancrenaz M, Marshall A, Goossens B et al (2008) Pongo pygmaeus. IUCN. www.iucnredlist.org. Accessed 18 May 2010

  4. Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103

    PubMed  Article  CAS  Google Scholar 

  5. Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242

    PubMed  Article  CAS  Google Scholar 

  6. Artacho E (2006) Reader-appeal should not outweigh merit of research. Nature 439:534

    PubMed  Article  CAS  Google Scholar 

  7. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Inc., Sunderland, MA

    Google Scholar 

  8. Baker A (2007) Animal ambassadors: an analysis of the effectiveness and conservation impact of ex situ breeding efforts. In: Zimmermann A, Hatchwell M, Dickie LA, West C (eds) Zoos in the 21st century—catalysts for conservation?, vol 15. Conservation biology. Cambridge University Press, Cambridge, pp 139–154

    Google Scholar 

  9. Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival & recovery. Analytical methods and strategies in small population conservation. Columbia University Press, New York

    Google Scholar 

  10. Barbará T, Palma-Silva C, Paggi GM et al (2007) Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol Ecol 16:3759–3767

    PubMed  Article  Google Scholar 

  11. Beauclerc KB, Johnson B, White BN (2010) Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (Peltophryne lemur) by mixing lineages. Conserv Genet 11:21–32

    Article  Google Scholar 

  12. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377

    PubMed  Article  CAS  Google Scholar 

  13. Birnbaum KD, Rosenbaum HC (2002) A practical guide for microsatellite analysis. In: DeSalle R, Giribet G, Wheeler W (eds) Techniques in molecular systematics and evolution. Birkhäuser-Verlag, Basel, pp 351–365

    Google Scholar 

  14. Blanc J (2008) Loxodonta africana. IUCN. www.iucnredlist.org. Accessed 24 Feb 2009

  15. Boakes EH, Wang JL (2005) A simulation study on detecting purging of inbreeding depression in captive populations. Genet Res 86:139–148

    PubMed  Article  Google Scholar 

  16. Boakes EH, Wang JL, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98:172–182

    PubMed  Article  CAS  Google Scholar 

  17. Bouman J (1977) The future of Przewalski horses (Equus przewalskii) in captivity. Int Zoo Yb 17:62–68

    Article  Google Scholar 

  18. Bowling AT, Zimmermann W, Ryder O et al (2003) Genetic variation in Przewalski’s horses, with special focus on the last wild caught mare, 231 Orlitza III. Cytogenet Genome Res 102:226–234

    PubMed  Article  CAS  Google Scholar 

  19. Butchart S, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168

    PubMed  Article  CAS  Google Scholar 

  20. Caballero A, Toro MA (2000) Interrelations between effective population size and other pedigree tools for the management of conserved populations. Genet Res 75:331–343

    PubMed  Article  CAS  Google Scholar 

  21. Conde DA, Flesness N, Colchero F et al (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390–1391

    PubMed  Article  CAS  Google Scholar 

  22. Conway W (2007) Entering the 21st century. In: Zimmermann A, Hatchwell M, Dickie LA, West C (eds) Zoos in the 21st century—catalysts for conservation?, vol 15. Conservation biology. Cambridge University Press, Cambridge, pp 12–21

    Google Scholar 

  23. Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    PubMed  Article  Google Scholar 

  24. Cuarón AD, de Grammont PC, Vázquez-Domínguez E et al (2008) Procyon pygmaeus. IUCN. www.iucnredlist.org. Accessed 11 Dec 2008

  25. de Guia APO, Saitoh T (2007) The gap between the concept and definitions in the Evolutionarily significant unit: the need to integrate neutral genetic variation and adaptive variation. Ecol Res 22:604–612

    Article  Google Scholar 

  26. Ellegren H (1999) Inbreeding and relatedness in Scandinavian grey wolves Canis lupus. Hereditas 130:239–244

    PubMed  Article  CAS  Google Scholar 

  27. Ellegren H, Savolainen P, Rosen B (1996) The genetical history of an isolated population of the endangered grey wolf Canis lupus: a study of nuclear and mitochondrial polymorphisms. Phil Trans Roy Soc Lond B Biol Sci 351:1661–1669

    Article  CAS  Google Scholar 

  28. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Harlow, England

    Google Scholar 

  29. Fickel J, Lieckfeldt D, Ratanakorn P et al (2007) Distribution of haplotypes and microsatellite alleles among Asian elephants (Elephas maximus) in Thailand. Eur J Wildl Res 53:298–303

    Article  Google Scholar 

  30. Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11

    Article  Google Scholar 

  31. Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825

    Article  Google Scholar 

  32. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    PubMed  Article  Google Scholar 

  33. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. University Press, Cambridge

    Google Scholar 

  34. Franklin IR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary—ecological perspective. Sinauer, Sunderland, MA, pp 135–150

    Google Scholar 

  35. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    PubMed  CAS  Google Scholar 

  36. Gautschi B, Muller JP, Schmid B et al (2003) Effective number of breeders and maintenance of genetic diversity in the captive bearded vulture population. Heredity 91:9–16

    PubMed  Article  CAS  Google Scholar 

  37. Gilligan DM, Frankham R (2003) Dynamics of genetic adaptation to captivity. Conserv Genet 4:189–197

    Article  Google Scholar 

  38. Gippoliti S, Amori G (2007) The problem of subspecies and biased taxonomy in conservation lists: the case of mammals. Folia Zoologica 56:113–117

    Google Scholar 

  39. Glenn TC, Dessauer HC, Braun MJ (1998) Characterization of microsatellite DNA loci in American alligators. Copeia 591–601

  40. Goncalves da Silva A, Lalonde DR, Quse V et al (2010) Genetic approaches refine ex situ Lowland Tapir (Tapirus terrestris) conservation. J Hered 101:581–590

    PubMed  Article  CAS  Google Scholar 

  41. Heath DD, Heath JW, Bryden CA et al (2003) Rapid evolution of egg size in captive salmon. Science 299:1738–1740

    PubMed  Article  CAS  Google Scholar 

  42. Hedrick PW (2005) Genetics of populations, 3rd edn. Jones & Bartlett Publishers, Sudbury

    Google Scholar 

  43. Hedrick PW, Fredrickson RJ (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350

    PubMed  Article  CAS  Google Scholar 

  44. Hedrick PW, Miller PS, Geffen E et al (1997) Genetic evaluation of the three captive Mexican wolf lineages. Zoo Biol 16:47–69

    Article  Google Scholar 

  45. Hedrick PW, Lee RN, Parker KM (2000) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity 85:617–624

    PubMed  Article  CAS  Google Scholar 

  46. Hochkirch A, Görzig Y (2009) Colonization and speciation on volcanic islands: phylogeography of the flightless grasshopper genus Arminda (Orthoptera, Acrididae) on the Canary Islands. Syst Entomol 34:188–197

    Article  Google Scholar 

  47. ISIS (2010) International Species Information System www.isis.org. Accessed 14 June 2010

  48. Ivy JA, Miller A, Lacy RC et al (2009) Methods and prospects for using molecular data in captive breeding programs: an empirical example using Parma wallabies (Macropus parma). J Hered 100:441–454

    PubMed  Article  Google Scholar 

  49. Jacobsen F, Nesje M, Bachmann L et al (2008) Significant genetic admixture after reintroduction of peregrine falcon (Falco peregrinus) in Southern Scandinavia. Conserv Genet 9:581–591

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  52. Kirkwood JK (2003) Welfare, husbandry and veterinary care of wild animals in captivity: Changes in attitude, progress in knowledge and techniques. Int Zoo Yb 38:124–130

    Article  Google Scholar 

  53. Kraaijeveld-Smit FJL, Griffiths RA, Moore RD et al (2006) Captive breeding and the fitness of reintroduced species: a test of the responses to predators in a threatened amphibian. J Appl Ecol 43:360–365

    Article  Google Scholar 

  54. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158

    Article  Google Scholar 

  55. Laikre L (1999a) Conservation genetics of Nordic carnivores: lessons from zoos. Hereditas 130:203–216

    PubMed  Article  CAS  Google Scholar 

  56. Laikre L (1999b) Hereditary defects and conservation genetic management of captive populations. Zoo Biol 18:81–99

    Article  Google Scholar 

  57. Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791

    Article  Google Scholar 

  58. Leader-Williams N, Balmford A, Linkie M et al (2007) Beyond the ark: conservation biologists’ views of the achievements of zoos in conservation. In: Zimmermann A, Hatchwell M, Dickie LA, West C (eds) Zoos in the 21st century—catalysts for conservation?, vol 15. Conservation biology. Cambridge University Press, Cambridge, pp 236–254

    Google Scholar 

  59. Leberg PL, Firmin BD (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17:334–343

    PubMed  Article  Google Scholar 

  60. Le Gouar P, Rigal F, Boisselier-Dubayle MC et al (2008) Genetic variation in a network of natural and reintroduced populations of Griffon vulture (Gyps fulvus) in Europe. Conserv Genet 9:349–359

    Article  Google Scholar 

  61. Mardis ER (2006) Anticipating the $1,000 genome. Genome Biol 7:5

    Article  Google Scholar 

  62. Marsden CD, Mable BK, Woodroffe R et al (2009) Highly endangered African wild dogs (Lycaon pictus) lack variation at the major histocompatibility complex. J Hered 100:S54–S65

    Article  CAS  Google Scholar 

  63. Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim Conserv 3:241–248

    Article  Google Scholar 

  64. Marshall TC, Sunnucks P, Spalton JA et al (1999) Use of genetic data for conservation management: the case of the Arabian oryx. Anim Conserv 2:269–278

    Article  Google Scholar 

  65. Maslin M (2006) Research skewed by stress on highest-impact journals. Nature 440:408

    PubMed  Article  CAS  Google Scholar 

  66. Maudet C, Miller C, Bassano B et al (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Mol Ecol 11:421–436

    Article  CAS  Google Scholar 

  67. Nielsen RK, Pertoldi C, Loeschcke V (2007) Genetic evaluation of the captive breeding program of the Persian wild ass. J Zool 272:349–357

    Article  Google Scholar 

  68. Norton JE, Ashley MV (2004) Genetic variability and population differentiation in captive Baird's tapirs (Tapirus bairdii). Zoo Biol 23:521–531

    Article  CAS  Google Scholar 

  69. O'Brien J, McCracken GF, Say L et al (2007) Rodrigues fruit bats (Pteropus rodricensis, Megachiroptera: Pteropodidae) retain genetic diversity despite population declines and founder events. Conserv Genet 8:1073–1082

    Article  Google Scholar 

  70. Pelletier F, Reale D, Watters J et al (2009) Value of captive populations for quantitative genetics research. Trends Ecol Evol 24:263–270

    PubMed  Article  Google Scholar 

  71. Princée FPG (2001) Genetic management of small animal populations. Lutra 44:103–112

    Google Scholar 

  72. R Development Core Team (2009) R: a language and environment for statistical computing. 2.8.1 edn. R Foundation for Statistical Computing, Vienna

  73. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544

    Article  Google Scholar 

  74. Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol Evol 1:19–22

    PubMed  Article  CAS  Google Scholar 

  75. Ralls K, Brugger K, Ballou JD (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206:1101–1103

    PubMed  Article  CAS  Google Scholar 

  76. Ramirez O, Altet L, Ensenat C et al (2006) Genetic assessment of the Iberian wolf Canis lupus signatus captive breeding program. Conserv Genet 7:861–878

    Article  Google Scholar 

  77. Robert A (2009) Captive breeding genetics and reintroduction success. Biol Conserv 142:2915–2922

    Article  Google Scholar 

  78. Ruiz-Lopez MJ, Roldan ERS, Espeso G et al (2009) Pedigrees and microsatellites among endangered ungulates: what do they tell us? Mol Ecol 18:1352–1364

    PubMed  Article  Google Scholar 

  79. Russello MA, Amato G (2004) Ex situ population management in the absence of pedigree information. Mol Ecol 13:2829–2840

    PubMed  Article  CAS  Google Scholar 

  80. Ryder A, Kumamoto AT, Durrant BS et al (1989) Chromosomal divergence and reproductive isolation in dik-diks. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, MA, pp 208–225

    Google Scholar 

  81. Sachdev M, Sankaranarayanan R, Reddanna P et al (2005) Major histocompatibility complex class I polymorphism in Asiatic lions. Tissue Antigens 66:9–18

    PubMed  Article  CAS  Google Scholar 

  82. Saura M, Perez-Figueroa A, Fernandez J et al (2008) Preserving population allele frequencies in ex situ conservation programs. Conserv Biol 22:1277–1287

    PubMed  Article  Google Scholar 

  83. Schmidt A (1999) Zur Ausbreitung von Waschbär Procyon lotor (L.) und Marderhund Nyctereutes procyonoides (Gray) in Ostbrandenburg (Ostdeutschland). Säugetierkundliche Mitteilungen 44:83–92

    Google Scholar 

  84. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    PubMed  Article  Google Scholar 

  85. Shen FJ, Zhang ZH, He W et al (2009) Microsatellite variability reveals the necessity for genetic input from wild giant pandas (Ailuropoda melanoleuca) into the captive population. Mol Ecol 18:1061–1070

    PubMed  Article  CAS  Google Scholar 

  86. Sigg DP (2006) Reduced genetic diversity and significant genetic differentiation after translocation: Comparison of the remnant and translocated populations of bridled nailtail wallabies (Onychogalea fraenata). Conserv Genet 7:577–589

    Article  Google Scholar 

  87. Signer EN, Schmidt CR, Jeffreys AJ (1994) DNA variability and parentage testing in captive Waldrapp ibises. Mol Ecol 3:291–300

    PubMed  Article  CAS  Google Scholar 

  88. Singleton I, Wich SA, Griffiths M (2008) Pongo abelii. IUCN. www.iucnredlist.org. Accessed 18 May 2010

  89. Smith S, Hughes J (2008) Microsatellite and mitochondrial DNA variation defines island genetic reservoirs for reintroductions of an endangered Australian marsupial, Perameles bougainville. Conserv Genet 9:547–557

    Article  CAS  Google Scholar 

  90. Smith S, McRae P, Hughes J (2009) Faecal DNA analysis enables genetic monitoring of the species recovery program for an arid-dwelling marsupial. Aust J Zool 57:139–148

    Article  Google Scholar 

  91. Snyder NFR, Derrickson SR, Beissinger SR et al (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348

    Article  Google Scholar 

  92. Soulé ME (1980) Thresholds for survival: maintaining fitness and evolutionary potential. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary—ecological perspective. Sinauer, Sunderland, MA, pp 151–169

    Google Scholar 

  93. Soulé ME, Gilpin M, Conway W et al (1986) The Millenium Ark: how long a voyage, how many staterooms, how many passengers? Zoo Biol 5:101–113

    Article  Google Scholar 

  94. Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180

    Article  Google Scholar 

  95. Tzika AC, Remy C, Gibson R et al (2009) Molecular genetic analysis of a captive-breeding program: the vulnerable endemic Jamaican yellow boa. Conserv Genet 10:69–77

    Article  CAS  Google Scholar 

  96. WAZA (2005) Building a future for wildlife—the world zoo and aquarium conservation strategy. WAZA

  97. WAZA (2010) Conservation breeding programs. www.waza.org. Accessed 14 June 2010

  98. Williams SE, Hoffman EA (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142:2388–2400

    Article  Google Scholar 

  99. Windig JJ, Kaal L (2008) An effective rotational mating scheme for inbreeding reduction in captive populations illustrated by the rare sheep breed Kempisch Heideschaap. Animal 2:1733–1741

    Article  Google Scholar 

  100. Wisely SM, McDonald DB, Buskirk SW (2003) Evaluation of the genetic management of the endangered black-footed ferret (Mustela nigripes). Zoo Biol 22:287–298

    Article  Google Scholar 

  101. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  CAS  Google Scholar 

  102. Xu QH, Fang SG, Wang ZP et al (2005) Microsatellite analysis of genetic diversity in the Chinese alligator (Alligator sinensis) Changxing captive population. Conserv Genet 6:941–951

    Article  CAS  Google Scholar 

  103. Zhi L, Karesh WB, Janczewski DN et al (1996) Genomic differentiation among natural populations of orang-utan (Pongo pygmaeus). Curr Biol 6:1326–1336

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is part of a PhD project that is financially supported by the Scholarship Programme of the German Federal Environmental Foundation. We thank Ann Hentschel for proofreading the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Axel Hochkirch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 71 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Witzenberger, K.A., Hochkirch, A. Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20, 1843–1861 (2011). https://doi.org/10.1007/s10531-011-0074-4

Download citation

Keywords

  • Genetic diversity
  • Inbreeding
  • Outbreeding
  • Population genetics
  • Reintroduction
  • Zoological garden