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.
Similar content being viewed by others
References
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
Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, Oxford, UK
Ancrenaz M, Marshall A, Goossens B et al (2008) Pongo pygmaeus. IUCN. www.iucnredlist.org. Accessed 18 May 2010
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
Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242
Artacho E (2006) Reader-appeal should not outweigh merit of research. Nature 439:534
Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, Inc., Sunderland, MA
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
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
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
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
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
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
Blanc J (2008) Loxodonta africana. IUCN. www.iucnredlist.org. Accessed 24 Feb 2009
Boakes EH, Wang JL (2005) A simulation study on detecting purging of inbreeding depression in captive populations. Genet Res 86:139–148
Boakes EH, Wang JL, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98:172–182
Bouman J (1977) The future of Przewalski horses (Equus przewalskii) in captivity. Int Zoo Yb 17:62–68
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
Butchart S, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168
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
Conde DA, Flesness N, Colchero F et al (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390–1391
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
Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Cuarón AD, de Grammont PC, Vázquez-Domínguez E et al (2008) Procyon pygmaeus. IUCN. www.iucnredlist.org. Accessed 11 Dec 2008
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
Ellegren H (1999) Inbreeding and relatedness in Scandinavian grey wolves Canis lupus. Hereditas 130:239–244
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
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Harlow, England
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
Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11
Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825
Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. University Press, Cambridge
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
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752
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
Gilligan DM, Frankham R (2003) Dynamics of genetic adaptation to captivity. Conserv Genet 4:189–197
Gippoliti S, Amori G (2007) The problem of subspecies and biased taxonomy in conservation lists: the case of mammals. Folia Zoologica 56:113–117
Glenn TC, Dessauer HC, Braun MJ (1998) Characterization of microsatellite DNA loci in American alligators. Copeia 591–601
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
Heath DD, Heath JW, Bryden CA et al (2003) Rapid evolution of egg size in captive salmon. Science 299:1738–1740
Hedrick PW (2005) Genetics of populations, 3rd edn. Jones & Bartlett Publishers, Sudbury
Hedrick PW, Fredrickson RJ (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350
Hedrick PW, Miller PS, Geffen E et al (1997) Genetic evaluation of the three captive Mexican wolf lineages. Zoo Biol 16:47–69
Hedrick PW, Lee RN, Parker KM (2000) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity 85:617–624
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
ISIS (2010) International Species Information System www.isis.org. Accessed 14 June 2010
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
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
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kimura M, Crow JF (1963) On the maximum avoidance of inbreeding. Genet Res 4:399–415
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
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
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
Laikre L (1999a) Conservation genetics of Nordic carnivores: lessons from zoos. Hereditas 130:203–216
Laikre L (1999b) Hereditary defects and conservation genetic management of captive populations. Zoo Biol 18:81–99
Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791
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
Leberg PL, Firmin BD (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17:334–343
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
Mardis ER (2006) Anticipating the $1,000 genome. Genome Biol 7:5
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
Marshall TC, Spalton JA (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim Conserv 3:241–248
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
Maslin M (2006) Research skewed by stress on highest-impact journals. Nature 440:408
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
Nielsen RK, Pertoldi C, Loeschcke V (2007) Genetic evaluation of the captive breeding program of the Persian wild ass. J Zool 272:349–357
Norton JE, Ashley MV (2004) Genetic variability and population differentiation in captive Baird's tapirs (Tapirus bairdii). Zoo Biol 23:521–531
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
Pelletier F, Reale D, Watters J et al (2009) Value of captive populations for quantitative genetics research. Trends Ecol Evol 24:263–270
Princée FPG (2001) Genetic management of small animal populations. Lutra 44:103–112
R Development Core Team (2009) R: a language and environment for statistical computing. 2.8.1 edn. R Foundation for Statistical Computing, Vienna
Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544
Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol Evol 1:19–22
Ralls K, Brugger K, Ballou JD (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206:1101–1103
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
Robert A (2009) Captive breeding genetics and reintroduction success. Biol Conserv 142:2915–2922
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
Russello MA, Amato G (2004) Ex situ population management in the absence of pedigree information. Mol Ecol 13:2829–2840
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
Sachdev M, Sankaranarayanan R, Reddanna P et al (2005) Major histocompatibility complex class I polymorphism in Asiatic lions. Tissue Antigens 66:9–18
Saura M, Perez-Figueroa A, Fernandez J et al (2008) Preserving population allele frequencies in ex situ conservation programs. Conserv Biol 22:1277–1287
Schmidt A (1999) Zur Ausbreitung von Waschbär Procyon lotor (L.) und Marderhund Nyctereutes procyonoides (Gray) in Ostbrandenburg (Ostdeutschland). Säugetierkundliche Mitteilungen 44:83–92
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
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
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
Signer EN, Schmidt CR, Jeffreys AJ (1994) DNA variability and parentage testing in captive Waldrapp ibises. Mol Ecol 3:291–300
Singleton I, Wich SA, Griffiths M (2008) Pongo abelii. IUCN. www.iucnredlist.org. Accessed 18 May 2010
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
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
Snyder NFR, Derrickson SR, Beissinger SR et al (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348
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
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
Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180
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
WAZA (2005) Building a future for wildlife—the world zoo and aquarium conservation strategy. WAZA
WAZA (2010) Conservation breeding programs. www.waza.org. Accessed 14 June 2010
Williams SE, Hoffman EA (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142:2388–2400
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
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
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159
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
Zhi L, Karesh WB, Janczewski DN et al (1996) Genomic differentiation among natural populations of orang-utan (Pongo pygmaeus). Curr Biol 6:1326–1336
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
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-011-0074-4