pp 1-20 | Cite as

Ex Situ Wildlife Conservation in the Age of Population Genomics

  • Michael A. Russello
  • Evelyn L. Jensen
Part of the Population Genomics book series


As the loss of biodiversity accelerates, there is general recognition that managing species outside of their native range (ex situ) will become increasingly important as populations continue to decline. Well-grounded in population genetic theory, ex situ conservation strategies, such as captive breeding, have largely relied on pedigree-based management out of both necessity and preference, despite known violations of important assumptions. Since the advent of molecular markers, many studies have successfully used empirical genetic data for informing ex situ conservation, yet their utility has been questioned due to competing priorities and resources as well as concerns related to potential biases associated with estimating individual- and population-level parameters based on traditional suites of loci. Paired with modern genotyping-by-sequencing approaches, population genomics holds great promise for overcoming past limitations associated with the use of empirical genetic data in ex situ conservation, allowing for highly precise estimates of population genetic parameters and identification of specific loci underlying traits of interest. Here, we review available literature and discuss the clear advantages and ultimate potential of using genome-wide data when managing species outside of their native range, from refining breeding decisions and assessing lineage integrity to minimizing adaptation to the captive environment and informing interactive in situ/ex situ conservation strategies. With resource-driven and capacity-related barriers to adoption falling away, our ability to harness leading-edge technologies to mine the genomes of wildlife species will enable more effective and efficient planning, implementation and monitoring of ex situ conservation strategies moving forward.


Ex situ population management Hybridization Introgression Reintroduction SNPs Species restoration 



We thank G. Amato and P. Hohenlohe for helpful comments on the manuscript. M.A.R acknowledges the support of the National Science and Engineering Research Council of Canada Discovery program (grant # 2014-04736). E.L.J. was supported by an NSERC Postgraduate Scholarship.


  1. Abbott RJ, Barton NH, Good JM. Genomics of hybridization and its evolutionary consequences. Mol Ecol. 2016;25:2325–32.Google Scholar
  2. Allendorf FW. Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol. 1986;5:181–90.Google Scholar
  3. Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nat Rev Genet. 2010;11:697–709.Google Scholar
  4. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet. 2016;17:81.Google Scholar
  5. Araki H, Cooper B, Blouin MS. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science. 2007;318:100–3.Google Scholar
  6. Attard C, Moller LM, Sasaki M, Hammer MP, Bice CM, Brauer CJ, et al. A novel holistic framework for genetic-based captive-breeding and reintroduction programs. Conserv Biol. 2016;30:1060–9.Google Scholar
  7. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One. 2008;3:e3376.Google Scholar
  8. Ballou JD. Calculating inbreeding coefficients from pedigrees. In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL, editors. Genetics and conservation: a reference for managing wild animal and plant populations. Menlo Park, CA: The Benjamin/Cummings Publishing Company, Inc; 1983. p. 509–21.Google Scholar
  9. Ballou JD, Lacy RC. Identifying genetically important individuals for management of genetic variation in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ, editors. Population management for survival and recovery. New York, NY: Columbia University Press; 1995. p. 76–111.Google Scholar
  10. Balmford A, Leader-Williams N, Green M. Parks or arks: where to conserve threatened mammals? Biodivers Conserv. 1995;4:595–607.Google Scholar
  11. Beck BB, Rapaport LG, Price MRS, Wilson AC. Reintroduction of captive-born animals. In: Olney PJS, Mace GM, Feistner ATC, editors. Creative conservation: interactive management of wild and captive animals. Dordrecht, The Netherlands: Springer; 1994. p. 265–86.Google Scholar
  12. Beheregaray LB, Pfeiffer LV, Attard CR, Sandoval-Castillo J, Domingos FM, Faulks LK, et al. Genome-wide data delimits multiple climate-determined species ranges in a widespread Australian fish, the golden perch (Macquaria ambigua). Mol Phylogenet Evol. 2017;111:65–75.Google Scholar
  13. Benirschke K. The frozen zoo concept. Zoo Biol. 1984;3:325–8.Google Scholar
  14. Black AN, Seears HA, Hollenbeck CM, Samollow PB. Rapid genetic and morphologic divergence between captive and wild populations of the endangered Leon Springs pupfish, Cyprinodon bovinus. Mol Ecol. 2017;26:2237–56.Google Scholar
  15. Blouin M, Parsons M, Lacaille V, Lotz S. Use of microsatellite loci to classify individuals by relatedness. Mol Ecol. 1996;5:393–401.Google Scholar
  16. Bowkett AE. Recent captive-breeding proposals and the return of the ark concept to global species conservation. Conserv Biol. 2009;23:773–6.Google Scholar
  17. Campbell NR, Harmon SA, Narum SR. Genotyping-in-thousands by sequencing (GT-seq): a cost effective SNP genotyping method based on custom amplicon sequencing. Mol Ecol Resour. 2015;15:855–67.Google Scholar
  18. CBSG. Tasmanian devil PHVA final report. Apple Valley: IUCN/SSC Conservation Breeding Specialist Group; 2008.Google Scholar
  19. Champagnon J, Elmberg J, Guillemain M, Gauthier-Clerc M, Lebreton J-D. Conspecifics can be aliens too: a review of effects of restocking practices in vertebrates. J Nat Conserv. 2012;20:231–41.Google Scholar
  20. Christie MR, Marine ML, French RA, Blouin MS. Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci U S A. 2012;109:238–42.Google Scholar
  21. Christie MR, Marine ML, Fox SE, French RA, Blouin MS. A single generation of domestication heritably alters the expression of hundreds of genes. Nat Commun. 2016;7.Google Scholar
  22. Çilingir FG, Rheindt FE, Garg KM, Platt K, Platt SG, Bickford DP. Conservation genomics of the endangered Burmese roofed turtle. Conserv Biol. 2017;31:1469–76.Google Scholar
  23. Clarke CN, Fraser DJ, Purchase CF. Lifelong and carry-over effects of early captive exposure in a recovery program for Atlantic salmon (Salmo salar). Anim Conserv. 2016;19:350–9.Google Scholar
  24. Conway WG. The practical difficulties and financial implications of endangered species breeding programmes. Int Zoo Yearb. 1986;24:210–9.Google Scholar
  25. Csilléry K, Johnson T, Beraldi D, Clutton-Brock T, Coltman D, Hansson B, et al. Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics. 2006;173:2091–101.Google Scholar
  26. Darwin C. The variation of animals and plants under domestication. London: John Murray; 1868.Google Scholar
  27. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 2011;12:499–510.Google Scholar
  28. De Bois H, Dhondt A, Van Puijenbroeck B. Effects of inbreeding on juvenile survival of the okapi Okapia johnstoni in captivity. Biol Conserv. 1990;54:147–55.Google Scholar
  29. Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, et al. Evolutionary genomics and conservation of the endangered Przewalski’s horse. Curr Biol. 2015;25:2577–83.Google Scholar
  30. Derrickson SR, Snyder NF. Potentials and limits of captive breeding in parrot conservation. New world parrots in crisis. Washington, DC: Smithsonian Institution Press; 1992. p. 133–63.Google Scholar
  31. Edwards T, Berry KH. Are captive tortoises a reservoir for conservation? An assessment of genealogical affiliation of captive Gopherus agassizii to local, wild populations. Conserv Genet. 2013;14:649–59.Google Scholar
  32. Ensslin A, Tschope O, Burkart M, Joshi J. Fitness decline and adaptation to novel environments in ex situ plant collections: current knowledge and future perspectives. Biol Conserv. 2015;192:394–401.Google Scholar
  33. Etter P, Bassham S, Hohenlohe PA, Johnson E, Cresko W. SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods Mol Biol. 2011;772:157–78.Google Scholar
  34. Fischer J, Lindenmayer DB. An assessment of the published results of animal relocations. Biol Conserv. 2000;96:1–11.Google Scholar
  35. Flesness NR. Gene pool conservation and computer analysis. Int Zoo Yearb. 1977;17:77–81.Google Scholar
  36. Foose T, Flesness N, Seal U, De Boer B, Rabb G. Ark into the 21st century. Apple Valley, MN: International Union for the Conservation of Nature and Natural Resources/Captive Breeding Specialist Group; 1992.Google Scholar
  37. Frankham R. Genetic adaptation to captivity in species conservation programs. Mol Ecol. 2008;17:325–33.Google Scholar
  38. Frankham R. Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv. 2010;143:1919–27.Google Scholar
  39. Frankham R, Loebel DA. Modeling problems in conservation genetics using captive Drosophila populations: rapid genetic adaptation to captivity. Zoo Biol. 1992;11:333–42.Google Scholar
  40. Frankham R, Ballou JD, Eldridge MD, Lacy RC, Ralls K, Dudash MR, et al. Predicting the probability of outbreeding depression. Conserv Biol. 2011;25:465–75.Google Scholar
  41. Fraser DJ. How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol Appl. 2008;1:535–86.Google Scholar
  42. Frazer NB. Sea turtle conservation and halfway technology. Conserv Biol. 1992;6:179–84.Google Scholar
  43. Gonçalves da Silva A, Lalonde DR, Quse V, Shoemaker A, Russello MA. Genetic approaches refine ex situ lowland tapir (Tapirus terrestris) conservation. J Hered. 2010;101:581–90.Google Scholar
  44. Grossen C, Biebach I, Angelone-Alasaad S, Keller LF, Croll D. Population genomics analyses of European ibex species show lower diversity and higher inbreeding in reintroduced populations. Evol Appl. 2018;11:123–39.Google Scholar
  45. Gruenthal KM, Witting DA, Ford T, Neuman MJ, Williams JP, Pondella DJ, et al. Development and application of genomic tools to the restoration of green abalone in southern California. Conserv Genet. 2014;15:109–21.Google Scholar
  46. Hammerly SC, de la Cerda DA, Bailey H, Johnson JA. A pedigree gone bad: increased offspring survival after using DNA-based relatedness to minimize inbreeding in a captive population. Anim Conserv. 2016;19:296–303.Google Scholar
  47. Hayes BJ, Lewin HA, Goddard ME. The future of livestock breeding: genomic selection for efficiency, reduced emissions intensity, and adaptation. Trends Genet. 2013;29:206–14.Google Scholar
  48. Heath DD, Heath JW, Bryden CA, Johnson RM, Fox CW. Rapid evolution of egg size in captive salmon. Science. 2003;299:1738–40.Google Scholar
  49. Hedrick PW. Conservation genetics: where are we now? Trends Ecol Evol. 2001;16:629–36.Google Scholar
  50. Henkel JR, Jones KL, Hereford SG, Savoie ML, Leibo S, Howard JJ. Integrating microsatellite and pedigree analyses to facilitate the captive management of the endangered Mississippi sandhill crane (Grus canadensis pulla). Zoo Biol. 2012;31:322–35.Google Scholar
  51. Henry P, Miquelle D, Sugimoto T, McCullough DR, Caccone A, Russello MA. In situ population structure and ex situ representation of the endangered Amur tiger. Mol Ecol. 2009;18:3173–84.Google Scholar
  52. Hoeck PEA, Wolak ME, Switzer RA, Kuehler CM, Lieberman AA. Effects of inbreeding and parental incubation on captive breeding success in Hawaiian crows. Biol Conserv. 2015;184:357–64.Google Scholar
  53. Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MA, et al. High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci U S A. 2014;111(10):3775–80.Google Scholar
  54. Howard JG, Lynch C, Santymire RM, Marinari PE, Wildt DE. Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Anim Conserv. 2016;19:102–11.Google Scholar
  55. Ishtiaq F, Prakash V, Green RE, Johnson J. Management implications of genetic studies for ex situ populations of three critically endangered Asian Gyps vultures. Anim Conserv. 2015;18:259–70.Google Scholar
  56. IUCN. The IUCN policy statement on captive breeding. Gland, Switzerland: IUCN; 1987.Google Scholar
  57. Ivy JA, Miller A, Lacy RC, DeWoody JA. Methods and prospects for using molecular data in captive breeding programs: an empirical example using parma wallabies (Macropus parma). J Hered. 2009;100:441–54.Google Scholar
  58. Ivy JA, Putnam AS, Navarro AY, Gurr J, Ryder OA. Applying SNP-derived molecular coancestry estimates to captive breeding programs. J Hered. 2016;107:403–12.Google Scholar
  59. Jensen EL, Tapia W, Caccone A, Russello MA. Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis ephippium). Conserv Genet. 2015;16:823–32.Google Scholar
  60. Jensen EL, Edwards DL, Garrick RC, Miller JM, Gibbs JP, Cayot LJ, et al. Population genomics through time provides insights into the consequences of decline and rapid demographic recovery through head-starting in a Galapagos giant tortoise. Evol Appl 2018 (in press).
  61. Johnson JA, Altwegg R, Evans DM, Ewen JG, Gordon IJ, Pettorelli N, et al. Is there a future for genome-editing technologies in conservation? Anim Conserv. 2016;19:97–101.Google Scholar
  62. Jones KL, Glenn TC, Lacy RC, Pierce JR, Unruh N, Mirande CM, et al. Refining the whooping crane studbook by incorporating microsatellite DNA and leg-banding analyses. Conserv Biol. 2002;16:789–99.Google Scholar
  63. Kleinman-Ruiz D, Martínez-Cruz B, Soriano L, Lucena-Perez M, Cruz F, Villanueva B, et al. Novel efficient genome-wide SNP panels for the conservation of the highly endangered Iberian lynx. BMC Genomics. 2017;18:556.Google Scholar
  64. Knief U, Schielzeth H, Backström N, Hemmrich-Stanisak G, Wittig M, Franke A, et al. Association mapping of morphological traits in wild and captive zebra finches: reliable within, but not between populations. Mol Ecol. 2017;26:1285–305.Google Scholar
  65. Kraaijeveld-Smit FJL, Griffiths RA, Moore RD, Beebee TJC. Captive breeding and the fitness of reintroduced species: a test of the responses to predators in a threatened amphibian. J Appl Ecol. 2006;43:360–5.Google Scholar
  66. Krohn AR, Conroy CJ, Pesapane R, Bi K, Foley JE, Rosenblum EB. Conservation genomics of desert dwelling California voles (Microtus californicus) and implications for management of endangered Amargosa voles (Microtus californicus scirpensis). Conserv Genet. 2018;19:383–95.Google Scholar
  67. Kyle R, Beatty GE, Roberts D, Provan J. Using genetic monitoring to inform best practice in a captive breeding programme: inbreeding and potential genetic rescue in the freshwater pearl mussel Margaritifera margaritifera. Conserv Genet. 2016;17:1323–32.Google Scholar
  68. Lacy RC. Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol. 1987;1:143–58.Google Scholar
  69. Lacy RC. Clarification of genetic terms and their use in the management of captive populations. Zoo Biol. 1995;14:565–77.Google Scholar
  70. Lermen D, Bloemeke B, Browne R, Clarke A, Dyce PW, Fixemer T, et al. Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Mol Ecol. 2009;18:1030–3.Google Scholar
  71. Lewis OT, Thomas CD. Adaptations to captivity in the butterfly Pieris brassicae (L.) and the implications for ex situ conservation. J Insect Conserv. 2001;5:55–63.Google Scholar
  72. Linnarsson S, Teichmann SA. Single-cell genomics: coming of age. Genome Biol. 2016;17:1–3.Google Scholar
  73. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 2003;4:981–94.Google Scholar
  74. MacCluer JW, VandeBerg JL, Read B, Ryder OA. Pedigree analysis by computer simulation. Zoo Biol. 1986;5:147–60.Google Scholar
  75. Martin MD, Jay F, Castellano S, Slatkin M. Determination of genetic relatedness from low-coverage human genome sequences using pedigree simulations. Mol Ecol. 2017;26(16):4145–57.Google Scholar
  76. Meffe GK. Techno-arrogance and halfway technologies: Salmon hatcheries on the Pacific coast of North America. Conserv Biol. 1992;6:350–4.Google Scholar
  77. Milián-García Y, Jensen EL, Madsen J, Álvarez Alonso S, Serrano Rodríguez A, Espinosa López G, et al. Founded: genetic reconstruction of lineage diversity and kinship informs ex situ conservation of Cuban Amazon parrots (Amazona leucocephala). J Hered. 2015a;106:573–9.Google Scholar
  78. Milián-García Y, Ramos-Targarona R, Perez-Fleitas E, Sosa-Rodriguez G, Guerra-Manchena L, Alonso-Tabet M, et al. Genetic evidence of hybridization between the critically endangered Cuban crocodile and the American crocodile: implications for population history and in situ/ex situ conservation. Heredity. 2015b;114:272–80.Google Scholar
  79. Miller JM, Quinzin MC, Poulakakis N, Gibbs JP, Beheregaray LB, Garrick RC, et al. Identification of genetically important individuals of the rediscovered Floreana Galápagos giant tortoise (Chelonoidis elephantopus) provide founders for Species Restoration Program. Sci Rep. 2017;7:11471.Google Scholar
  80. Mitchell AA, Lau J, Chemnick LG, Thompson EA, Alberts AC, Ryder OA, et al. Using microsatellite diversity in wild Anegada iguanas (Cyclura pinguis) to establish relatedness in a captive breeding group of this critically endangered species. Conserv Genet. 2011;12:771–81.Google Scholar
  81. Myers N. The sinking ark: a new look at the problem of disappearing species. Oxford, UK: Pergamon Press; 1979. 307 p.Google Scholar
  82. Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA. Genotyping-by-sequencing in ecological and conservation genomics. Mol Ecol. 2013;22:2841–7.Google Scholar
  83. Oliveira R, Randi E, Mattucci F, Kurushima JD, Lyons LA, Alves PC. Toward a genome-wide approach for detecting hybrids: informative SNPs to detect introgression between domestic cats and European wildcats (Felis silvestris). Heredity. 2015;115:195–205.Google Scholar
  84. Oliveira PRR, Costa MC, Silveira LF, Francisco MR. Genetic guidelines for captive breeding and reintroductions of the endangered Black-fronted Piping Guan, Aburria jacutinga (galliformes, cracidae), an Atlantic Forest endemic. Zoo Biol. 2016;35:313–8.Google Scholar
  85. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One. 2012;7:e37135.Google Scholar
  86. Philippart JC. Is captive breeding an effective solution for the preservation of endemic species? Biol Conserv. 1995;72:281–95.Google Scholar
  87. Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science. 2014;344:1246752.Google Scholar
  88. Price MR, Sischo D, Pascua MA, Hadfield MG. Demographic and genetic factors in the recovery or demise of ex situ populations following a severe bottleneck in fifteen species of Hawaiian tree snails. PeerJ. 2015;3:e1406.Google Scholar
  89. Rahbek C. Captive breeding – a useful tool in the preservation of biodiversity? Biodivers Conserv. 1993;2:426–37.Google Scholar
  90. Ralls K, Ballou J. Extinction: lessons from zoos. In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL, editors. Genetics and conservation: a reference for managing wild animal and plant populations. Menlo Park, CA: The Benjamin/Cummings Publishing Company, Inc.; 1983. p. 164–84.Google Scholar
  91. Ralls K, Ballou JD, Rideout BA, Frankham R. Genetic management of chondrodystrophy in California condors. Anim Conserv. 2000;3:145–53.Google Scholar
  92. Ray JW, King RB, Duvall MR, Robinson JW, Jaeger CP, Dreslik MJ, et al. Genetic analysis and captive breeding program design for the eastern massasauga Sistrurus catenatus catenatus. J Fish Wildl Manag. 2013;4:104–13.Google Scholar
  93. Ritland K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res. 1996;67:175–85.Google Scholar
  94. Russello MA, Amato G. Ex situ population management in the absence of pedigree information. Mol Ecol. 2004;13:2829–40.Google Scholar
  95. Russello MA, Amato G. On the horns of a dilemma: molecular approaches refine ex situ conservation in crisis. Mol Ecol. 2007;16:2405–6.Google Scholar
  96. Russello MA, Hyseni C, Gibbs JP, Cruz S, Marquez C, Tapia W, et al. Lineage identification of Galápagos tortoises in captivity worldwide. Anim Conserv. 2007;10:304–11.Google Scholar
  97. Russello MA, Poulakakis N, Gibbs JP, Tapia W, Benavides E, Powell JR, et al. DNA from the past informs ex situ conservation for the future: an “extinct” species of Galápagos tortoise identified in captivity. PLoS One. 2010a;5:e8683.Google Scholar
  98. Russello MA, Stahala C, Lalonde D, Schmidt KL, Amato G. Cryptic diversity and conservation units in the Bahama parrot. Conserv Genet. 2010b;11:1809–21.Google Scholar
  99. Ryder O, Miller W, Ralls K, Ballou JD, Steiner CC, Mitelberg A, et al. Whole genome sequencing of California condors is now utilized for guiding genetic management. International Plant and Animal Genome XXIV Conference; 8–13 Jan 2016, San Diego, CA, USA.Google Scholar
  100. Saragusty J, Diecke S, Drukker M, Durrant B, Friedrich Ben-Nun I, Galli C, et al. Rewinding the process of mammalian extinction. Zoo Biol. 2016;35:280–92.Google Scholar
  101. Seal U, Foose T, Ellis S. Conservation assessment and management plans (CAMPs) and global captive action plans (GCAPs). Creative conservation: interactive management of wild and captive animals. Dordrecht, The Netherlands: Springer; 1994. p. 312–25.Google Scholar
  102. Snyder NFR, Derrickson SR, Beissinger SR, Wiley JW, Smith TB, Toone WD, et al. Limitations of captive breeding in endangered species recovery. Conserv Biol. 1996;10:338–48.Google Scholar
  103. Soulé ME, Simberloff D. What do genetics and ecology tell us about the design of nature reserves? Biol Conserv. 1986;35:19–40.Google Scholar
  104. Speed D, Balding DJ. Relatedness in the post-genomic era: is it still useful? Nat Rev Genet. 2015;16:33–44.Google Scholar
  105. Strzala T, Kowalczyk A, Lukaszewicz E. Reintroduction of the European capercaillie from the Capercaillie Breeding Centre in Wisla Forest District: genetic assessments of captive and reintroduced populations. PLoS One. 2015;10:13.Google Scholar
  106. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet. 2008;9:465–76.Google Scholar
  107. Svengren H, Prettejohn M, Bunge D, Fundi P, Bjorklund M. Relatedness and genetic variation in wild and captive populations of Mountain Bongo in Kenya obtained from genome-wide single-nucleotide polymorphism (SNP) data. Glob Ecol Conserv. 2017;11:196–206.Google Scholar
  108. Tear TH, Scott JM, Hayward PH, Griffith B. Status and prospects for success of the Endangered Species Act. Science. 1993;262:976–7.Google Scholar
  109. Therkildsen NO, Palumbi SR. Practical low-coverage genomewide sequencing of hundreds of individually barcoded samples for population and evolutionary genomics in nonmodel species. Mol Ecol Resour. 2017;17:194–208.Google Scholar
  110. Thompson EA. Pedigree analysis in human genetics. Baltimore: Johns Hopkins University Press; 1986.Google Scholar
  111. Tokarska M, Marshall T, Kowalczyk R, Wójcik J, Pertoldi C, Kristensen T, et al. Effectiveness of microsatellite and SNP markers for parentage and identity analysis in species with low genetic diversity: the case of European bison. Heredity. 2009;103:326–32.Google Scholar
  112. Tudge C. Last animals at the zoo: how mass extinction can be stopped. Washington, DC: Island Press; 1992. 265 p.Google Scholar
  113. Tunstall T, Kock R, Vahala J, Diekhans M, Fiddes I, Armstrong J, et al. Evaluating recovery potential of the northern white rhinoceros from cryopreserved somatic cells. Genome Res. 2018;28(6):780–8.Google Scholar
  114. Urano K, Tsubono K, Taniguchi Y, Matsuda H, Yamada T, Sugiyama T, et al. Genetic diversity and structure in the Sado captive population of the Japanese crested ibis. Zoolog Sci. 2013;30:432–8.Google Scholar
  115. Valbuena-Urena E, Soler-Membrives A, Steinfartz S, Alonso M, Carbonell F, Larios-Martin R, et al. Getting off to a good start? Genetic evaluation of the ex situ conservation project of the Critically Endangered Montseny brook newt (Calotriton arnoldi). PeerJ. 2017;5:25.Google Scholar
  116. Van de Casteele T, Galbusera P, Matthysen E. A comparison of microsatellite-based pairwise relatedness estimators. Mol Ecol. 2001;10:1539–49.Google Scholar
  117. Waters CD, Hard JJ, Brieuc MSO, Fast DE, Warheit KI, Waples RS, et al. Effectiveness of managed gene flow in reducing genetic divergence associated with captive breeding. Evol Appl. 2015;8:956–71.Google Scholar
  118. West R, Potter S, Taggart D, Eldridge MDB. Looking back to go forward: genetics informs future management of captive and reintroduced populations of the black-footed rock-wallaby Petrogale lateralis. Conserv Genet. 2018;19:235–47.Google Scholar
  119. Willoughby JR, Ivy JA, Lacy RC, Doyle JM, DeWoody JA. Inbreeding and selection shape genomic diversity in captive populations: implications for the conservation of endangered species. PLoS One. 2017;12.Google Scholar
  120. Witzenberger KA, Hochkirch A. The genetic integrity of the ex situ population of the European wildcat (Felis silvestris silvestris) is seriously threatened by introgression from domestic cats (Felis silvestris catus). PLoS One. 2014;9(8):e106083.Google Scholar
  121. Wright S. Systems of mating. II. The effects of inbreeding on the genetic composition of a population. Genetics. 1921;6:124–43.Google Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyThe University of British ColumbiaKelownaCanada

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