The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations

Molecular Ecology

Volumn 24, Issue 1, 2015, Pages 98-110

  Willoughby, Janna R ^a   Fernandez, Nadia B ^b   Lamb, Maureen C ^b   Ivy, Jamie A ^c   Lacy, Robert C ^d   Dewoody, J Andrew ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c Global Collections Department San Diego Zoo   (United States)

^d BROOKFIELD ZOO   (United States)

Author keywords

Adaptation; Docility; Mean kinship; microsatellite; mitochondrial DNA; pedigree

Indexed keywords

PEROMYSCUS;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ALLELE; ANIMAL; BIOLOGICAL MODEL; BREEDING; COMPUTER SIMULATION; ENVIRONMENTAL PROTECTION; GENETIC DRIFT; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; INBREEDING; MOLECULAR GENETICS; PEDIGREE; PEROMYSCUS; PROCEDURES;

ALLELES; ANIMALS; BREEDING; COMPUTER SIMULATION; CONSERVATION OF NATURAL RESOURCES; DNA, MITOCHONDRIAL; GENETIC DRIFT; GENETIC VARIATION; HAPLOTYPES; INBREEDING; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PEDIGREE; PEROMYSCUS; SELECTION, GENETIC;

EID: 84920816378     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13020     Document Type: Article

References (65)

1. Allendorf F, Luikart G, (2007) Conservation and the Genetics of Populations. Blackwell Publishing, Oxford, UK.
2. Ballou JD, Lacy RC, (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Population Management for Survival and Recovery (eds, Ballou JD, Fooze TJ, Gilpin M,), pp. 76-111. Columbia University Press, New York.
3. Boakes EH, Wang KL, Amos W, (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity, 98, 172-182.
4. Bulut Z, McCormick CR, Gopurenko D, Williams RN, Bos DH, DeWoody JA, (2009) Microsatellite mutation rates in the eastern tiger salamander (Ambystoma tigrinum tigrinum) differ 10-fold across loci. Genetica, 136, 501-504.
5. Canty A, Ripley B, (2014) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-11.Coster A. 2012. pedigree: Pedigree functions. R package version 1.4. Available at: http://CRAN.R-project.org/package=pedigree.
6. Chirhart SE, Honeycutt RL, Greenbaum IF, (2000) Microsatellite markers for the deer mouse Peromyscus maniculatus. Molecular Ecology, 9, 1669-1671.
7. Coster A, (2013) pedigree: Pedigree functions. R package version 1.4. Available from: http://CRAN.R-project.org/package=pedigree.
8. Crow JF, Denniston C, (1988) Inbreeding and variance effective population numbers. Evolution, 42, 482-495.
9. Crow JF, Kimura M, (1970) Introduction to Population Genetics Theory. Harper & Row, Publishers, New York.
10. Dallas JF, (1992) Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mammalian Genome, 3, 452-456.
11. Davison AC, Hinkley DV, (1997) Bootstrap Methods and Their Applications. Cambridge University Press, Cambridge.
12. DeWoody YD, DeWoody JA, (2005) On the estimation of genome-wide heterozygosity using molecular markers. Journal of Heredity, 96, 85-88.
13. van Dierendonck MC, Wallis de Vries MF, (1996) Ungulate reintroductions: experiences with the Takhi or Przewalski Horse (Equus ferus przewalskii) in Mongolia. Conservation Biology, 10, 728-740.
14. Doyle RW, Perez-Enriquez R, Takagi M, Taniguchi N, (2001) Selective recovery of founder genetic diversity in aquacultural broodstocks and captive, endangered fish populations. Genetica, 111, 291-304.
15. Fernandez J, Toro MA, Caballero A, (2004) Managing individuals' contributions to maximize the allelic diversity maintained in small, conserved populations. Conservation Biology, 18, 1358-1367.
16. Fisch KM, Ivy JA, Burton RS, May B, (2013) Evaluating the performance of captive breeding techniques for conservation hatcheries: a case study of the delta smelt captive breeding program. Journal of Heredity, 104, 92-104.
17. Fischer J, Lindenmayer DB, (2000) An assessment of the published results of animal relocations. Biological Conservation, 96, 1-11.
18. Fisher RA, (1919) The correlation between relatives on the supposition of mendelian inheritance. Transactions of the Royal Society of Edinburgh, 52, 399-433.
19. Forstmeier W, Segelbacher G, Mueller JC, Kempenaers B, (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Molecular Ecology, 19, 4039-4050.
20. Frankham R, (2008) Genetic adaptation to captivity in species conservation programs. Molecular Ecology, 17, 325-333.
21. Frankham R, Loebel DA, (1992) Modeling problems in conservation genetics using captive Drosophila populations-rapid genetic adaptation to captivity. Zoo Biology, 11, 333-342.
22. Frankham R, Manning H, Margan SH, Briscoe DA, (2006) Does equalization of family sizes reduce genetic adaptation to captivity? Animal Conservation, 3, 357-363.
23. Hanski I, Saccheri I, (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biology, 4, e129.
24. Ivy JA, Lacy RC, (2010) Using molecular method to improve the genetic management of captive breeding programs for threatened species. In: Molecular Approaches in Natural Resource Conservation and Management (eds, DeWoody JA, Bickham JW, Michler CH, Nichols KM, Rhodes OE, Woeste KE,), pp. 267-295. Cambridge University Press, Cambridge.
25. Ivy JA, Lacy RC, (2012) A comparison of strategies for selecting breeding pairs to maximize genetic diversity retention in managed populations. Journal of Heredity, 103, 186-196.
26. Lachance S, Magnan P, (1990) Performance of domestic, hybrid, and wild strains of brook trout, Salvelinus fontinalis, after stocking: the impact of intraspecific and interspecific competition. Canadian Journal of Fisheries and Aquatic Sciences, 47, 2278-2284.
27. Lacy RC, (1994) Managing genetic diversity in captive populations of animals. In: Restoration of Endangered Species: Conceptual Issues, Planning and Implementation (eds, Bowles ML, Whelan CJ,), pp. 63-89. Cambridge University Press, Cambridge.
28. Lacy RC, (1995) Clarification of genetic terms and their use in the management of captive populations. Zoo Biology, 14, 565-577.
29. Lacy RC, (2000) Should we select genetic alleles in our conservation breeding programs? Zoo Biology, 19, 279-282.
30. Lacy RC, (2009) Stopping evolution: genetic management of captive populations. In: Conservation Genetics in the Age of Genomics (eds, Amato G, DeSalle R, Ryder OA, Rosenbaum HC,), pp. 58-81. Columbia University Press, New York.
31. Lacy RC, (2012) Achieving true sustainability of zoo populations. Zoo Biology, 32, 19-26.
32. Lacy RC, Ballou JD, Pollak JP, (2012) PMx: Software package for demographic and genetic analysis and management of pedigreed populations. Methods in Ecology & Evolution, 3, 433-437.
33. Lacy RC, Alaks G, Walsh A, (2013) Evolution of Peromyscus leucopus mice in response to a captive environment. PLos One, 8, e72452.
34. Leberg PL, (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution, 46, 477-494.
35. Leus K, Traylor-Holzer K, Lacy RC, (2011) Genetic and demographic population management in zoos and aquariums: recent developments, future challenges and opportunities for scientific research. International Zoo Yearbook, 45, 213-225.
36. McPhee ME, (2004) Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs. Biological Conservation, 115, 71-77.
37. Melampy MN, Howe HF, (1977) Sex-ratio in tropical tree Triplaris americana (Polygonaceae). Evolution, 31, 867-872.
38. Miller B, Biggins D, Hanebury L, Vargas A, (1994) Reintroduction of the Black-footed ferret (Mustela nigripes). In: Creative Conservation: Interactive Management of Wild and Captive Animals (eds, Olney PJS, Mace GM, Feistner ATC,), pp. 455-464. Chapman & Hall, New York.
39. Montgomery ME, Ballou JD, Nurthen RK, England PR, Briscoe DA, Frankham R, (1997) Minimizing kinship in captive breeding programs. Zoo Biology, 16, 377-389.
40. Montgomery ME, Woodworth LM, England PR, Brisco DA, Frankham R, (2010) Widespread selective sweeps affecting microsatellites in Drosophila populations adapting to captivity: implications for captive breeding programs. Biological Conservation, 143, 1842-1849.
41. Moorhouse TP, Gelling M, Macdonald DW, (2009) Effects of habitat quality upon reintroduction success in water voles: evidence from a replicated experiment. Biological Conservation, 142, 53-60.
42. Morzunov SP, Rowe JE, Ksiazek TG, Peters CJ, St. Jeor SC, Nichol ST, (1998) Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. Journal of Virology, 72, 57-64.
43. Mullen LM, Hirschmann RJ, Prince KL, Glenn TC, Dewey MJ, Hoekstra HE, (2006) Sixty polymorphic microsatellite markers for the oldfield mouse developed in Peromyscus polionotus and Peromyscus maniculatus. Molecular Ecology Notes, 6, 36-40.
44. Nei M, Li W-H, (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Science, 76, 5269-5273.
45. Nei M, Tajima F, (1981) DNA polymorphism detectable by restriction endonucleases. Genetics, 97, 145.
46. Ortega-Villaizan MD, Noguchi D, Taniguchi N, (2011) Minimization of genetic diversity loss of endangered fish species captive broodstocks by means of minimal kinship selective crossbreeding. Aquaculture, 318, 239-243.
47. Paquette SR, (2012) PopGenKit: Useful functions for (batch) file conversion and data resampling in microsatellite datasets. R package version 1.0. Available from: http://CRAN.R-project.org/package=PopGenKit.
48. Prince KL, Glenn TL, Dewey MJ, (2002) Cross-species amplification among peromyscines of new microsatellite DNA loci from the oldfield mouse (Peromyscus polionotus subgriseus). Molecular Ecology Notes, 2, 133-136.
49. Queller DC, Goodnight KF, (1989) Estimating relatedness using genetic markers. Evolution, 43, 258-275.
50. Rafinesque CS, (1818) Further discoveries in natural history, made during a journey through the western region of the United States. American Monthly Magazine, 3, 445-447.
51. Ritland K, (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genetical Research, 67, 175-185.
52. Rudnick JA, Miller A, Lacy RC, DeWoody JA, (2009) Methods and prospects for using molecular data in the genetic management of populations: an empirical example using parma wallabies (Macropus parma). Journal of Heredity, 100, 441-454.
53. Russell WC, Thorne ET, Oakleaf R, Ballou JD, (1994) The genetic-basis of black-footed ferret reintroduction. Conservation Biology, 8, 263-266.
54. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I, (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
55. Sambrook J, Russell DW, (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
56. Schmidt C, (1999) Variation and congruence of microsatellite markers for Peromyscus leucopus. Journal of Mammalogy, 80, 522-529.
57. Sonesson AK, Meuwissen THE, (2000) Mating schemes for optimum contribution selection with constrained rates of inbreeding. Genetics Selection Evolution, 32, 231-248.
58. Stanley Price MR, (1989) Animal Re-Introductions: The Arabian oryx in Oman. Cambridge University Press, Cambridge.
59. Therneau T, Atkinson E, Sinnwell J, Schaid D, McDonnell S, (2014) kinship2: Pedigree functions. R package version 1.5.7. Available from: http://CRAN.R-project.org/package=kinship2.
60. Toone WD, Wallace MP, (1994) The extinction in the wild and reintroduction of the California condor (Gymnogyps californianus). In: Creative Conservation: Interactive Management of Wild and Captive Animals (eds, Olney PJS, Mace GM, Feistner ATC,), pp. 411-419. Chapman & Hall, New York.
61. Utter F, Epifanio J, (2002) Marine aquaculture: genetic potentialities and pitfalls. Reviews in Fish Biology and Fisheries, 12, 59-77.
62. Vila C, Sundqvist AK, Flagstad O, et al,. (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society B: Biological Sciences, 270, 91-97.
63. Waples RS, (1991) Genetic interactions between hatchery and wild salmonids: lessons from the Pacific Northwest. Canadian Journal of Fisheries and Aquatic Sciences, 48, 124-133.
64. Williams SE, Hoffman EA, (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biological Conservation, 142, 2388-2400.
65. Woodworth LM, Montgomery ME, Briscoe DA, Frankham R, (2002) Rapid genetic deterioration in captive populations: causes and conservation implications. Conservation Genetics, 3, 277-288.