The Genetics of Reintroductions: Inbreeding and Genetic Drift

Reintroduction Biology: Integrating Science and Management

Volumn , Issue , 2012, Pages 360-394

  Keller, Lukas F ^a   Biebach, Iris ^a   Ewing, Steven R ^b   Hoeck, Paquita E A ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b RSPB CENTRE FOR CONSERVATION SCIENCE   (United Kingdom)

Author keywords

Genetic drift, allele frequency changes; Genetics of reintroductions, genetic drift; Inbreeding depression; Inbreeding in conservation biology; Inbreeding, loss of genetic variation; Inbreeding, under random mating; Measuring inbreeding; Population dynamics; Reintroduced, and genetic drift effects; Reintroduction

Indexed keywords

EID: 84863496717     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444355833.ch11     Document Type: Chapter

References (121)

1. Allendorf, F.W. & Luikart, G. (2007) Conservation and the Genetics of Populations. Blackwell, Malden, Massachusetts, USA.
2. Armbruster, P. & Reed, D.H. (2005) Inbreeding depression in benign and stressful environments. Heredity, 95, 235-242.
3. Armstrong, D.P., Davidson, R.S., Perrott, J.K. et al. (2005) Density-dependent population growth in a reintroduced population of North Island saddlebacks. Journal of Animal Ecology, 74, 160-170.
4. Ballou, J.D. (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. Journal of Heredity, 88, 169-178.
5. Bataillon, T. & Kirkpatrick, M. (2000) Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genetical Research, 75, 75-81.
6. Biebach, I. & Keller, L.F. (2009) A strong genetic footprint of the re-introduction history of Alpine ibex (Capra ibex ibex). Molecular Ecology, 18, 5046-5058.
7. Biebach, I. & Keller, L.F. (2010) Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Conservation Genetics, 11, 527-538.
8. Bijlsma, R., Bundgaard, J. & van Putten, W.F. (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology, 12, 1125-1137.
9. Bijlsma, R., Bundgaard, J.&Boerema, A.C. (2000) Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. Journal of Evolutionary Biology, 13, 502-514.
10. Boakes, E.H., Wang, J. & Amos, W. (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity, 98, 172-182.
11. Brekke, P., Bennett, P.M., Wang, J.L. et al. (2010) Sensitive males: inbreeding depression in an endangered bird. Proceedings of the Royal Society of London B, 277, 3677-3684.
12. Broders, H.G., Mahoney, S.P., Montevecchi, W.A. et al. (1999) Population genetic structure and the effect of founder events on the genetic variability of moose, Alces alces, in Canada. Molecular Ecology, 8, 1309-1315.
13. Byers, D.L. & Waller, D.M. (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics, 30, 479-513.
14. Caballero, A. (1994) Developments in the prediction of effective population size. Heredity, 73, 657-679.
15. Caro, T.M. & Laurenson, M.K. (1994) Ecological and genetic factors in conservation: a cautionary tale. Science, 263, 485-486.
16. Charlesworth, B. (2009) Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics, 10, 195-205.
17. Charlesworth, D.&Willis, J.H. (2009) Fundamental concepts in genetics-the genetics of inbreeding depression. Nature Reviews Genetics, 10, 783-796.
18. Charman, T.G., Sears, J., Green, R.E. et al. (2010) Conservation genetics, foraging distance and nest density of the scarce great yellow bumblebee (Bombus distinguendus). Molecular Ecology, 19, 2661-2674.
19. Comstock, R.E. & Winters, L.M. (1944) A comparison of the effects of inbreeding and selection on performance in swine. Journal of Animal Science, 3, 380-389.
20. Crnokrak, P. & Barrett, S.C.H. (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution, 56, 2347-2358.
21. Crnokrak, P. & Roff, D.A. (1999) Inbreeding depression in the wild. Heredity, 83, 260-270.
22. Crow, J.F. (1980) The estimation of inbreeding from isonymy. Human Biology, 52, 1-14.
23. Crow, J.F. (2010) Wright and Fisher on inbreeding and random drift. Genetics, 184, 609-611.
24. Crow, J.F. & Kimura, M. (1970) An Introduction to Population Genetics Theory. Burgess Publishing Company, Minneapolis, Minnesota, USA.
25. Darwin, C. (1868) The Variation of Animals and Plants under Domestication. J. Murray and Co., London, UK.
26. Darwin, C. (1876) The Effects of Cross and Self Fertilization in the Vegetable Kingdom. J. Murray and Co, London, UK.
27. DeRose, M.A. & Roff, D.A. (1999) A comparison of inbreeding depression in lifehistory and morphological traits in animals. Evolution, 53, 1288-1292.
28. Ewen, J.G., Acevedo-Whitehouse, K., Alley, M. et al. (2011) Empirical consideration of parasites and health in reintroduction. In Reintroduction Biology: integrating science and management, eds J.G. Ewen, D.P. Armstrong, K.A. Parker & P.J. Seddon, Chapter 9. Wiley-Blackwell, Oxford, UK.
29. Ewing, S.R., Nager, R.G., Nicoll, M.A.C. et al. (2008) Inbreeding and loss of genetic variation in a reintroduced population of Mauritius kestrel. Conservation Biology, 22, 395-404.
30. Ewen, J.G., Thorogood, R. & Armstrong, D.P. (2011) Demographic consequences of adult sex ratio in a reintroduced hihi population. Journal of Animal Ecology, 80, 448-455.
31. Ficetola, G.F., Garner, T.W.J., Wang, J.L. et al. (2011) Rapid selection against inbreeding in a wild population of a rare frog. Evolutionary Applications, 4, 30-38.
32. Fox, C.W. (2005) Problems in measuring among-family variation in inbreeding depression. American Journal of Botany, 92, 1929-1932.
33. Frankham, R. (2008) Genetic adaptation to captivity in species conservation programs. Molecular Ecology, 17, 325-333.
34. Frankham, R., Ballou, J.D.&Briscoe, D.A. (2002) Introduction to Conservation Genetics. Cambridge University Press, Cambridge, UK.
35. Frankham, R., Gilligan, D.M., Morris, D. et al. (2001) Inbreeding and extinction: effects of purging. Conservation Genetics, 2, 279-285.
36. Frankham, R., Lees, K., Montgomery, M.E. et al. (1999) Do population size bottlenecks reduce evolutionary potential? Animal Conservation, 2, 255-260.
37. Fredrickson, R.J., Siminski, P., Woolf, M. et al. (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proceedings of the Royal Society of London B, 274, 2365-2371.
38. Gaggiotti, O. E. (2003) Genetic threats to population persistence. Annales Zoologici Fennici, 40, 155-168.
39. Gaggiotti, O.E.&Couvet, D. (2004) Genetic structure in heterogeneous environments. In Evolutionary Conservation Biology, eds R. Ferrière, U. Dieckmann & D. Couvet, pp. 229-243. Cambridge University Press, Cambridge, UK.
40. Glémin, S. (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution, 57, 2678-2687.
41. Glémin, S. (2007) Mating systems and the efficacy of selection at the molecular level. Genetics, 177, 905-916.
42. Glémin, S., Ronfort, J. & Bataillon, T. (2003) Patterns of inbreeding depression and architecture of the load in subdivided populations. Genetics, 165, 2193-2212.
43. Groombridge, J.J., Raisin, C., Bristol, R. et al. (2011) Genetic consequences of reintroductions and insights from population history. In Reintroduction Biology: integrating science and management, eds J.G. Ewen, D.P. Armstrong, K.A. Parker & P.J. Seddon, Chapter 12. Wiley-Blackwell, Oxford, UK.
44. Grøtan, V., Sæther, B.E., Filli, F. et al. (2008) Effects of climate on population fluctuations of ibex. Global Change Biology, 14, 218-228.
45. Gulisija, D., Gianola, D., Weigel, K.A. et al. (2006) Between-founder heterogeneity in inbreeding depression for production in Jersey cows. Livestock Science, 104, 244-253.
46. Haig, S.M. & Ballou, J.D. (2002) Pedigree analyses of wild populations. In Population Viability Analysis, eds S.R. Beissinger & D.R. McCullough, pp. 388-405. The University of Chicago Press, Chigago, Illinois, USA.
47. Hedrick, P.W. (1994) Purging inbreeding depression and the probability of extinction-full-sib mating. Heredity, 73, 363-372.
48. Hedrick, P.W. (2000) Genetics of Populations. Jones and Bartlett, Boston, Massachusetts, USA.
49. Hedrick, P.W. (2001) Conservation genetics: where are we now? Trends in Ecology & Evolution, 16, 629-636.
50. Hedrick, P.W. & Kalinowski, S.T. (2000) Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics, 31, 139-162.
51. Hedrick, P.W. & Miller, P.S. (1992) Conservation genetics-techniques and fundamentals. Ecological Applications, 2, 30-46.
52. Hoeck, P.E.A., Bollmer, J.L., Parker, P.G. et al. (2010) Differentiation with drift: a spatio-temporal genetic analysis of Galapagos mockingbird populations (Mimus spp.). Philosophical Transactions of the Royal Society of London B, 365, 1127-1138.
53. Hogg, J.T., Forbes, S.H., Steele, B.M. et al. (2006) Genetic rescue of an insular population of large mammals. Proceedings of the Royal Society of London B, 273, 1491-1499.
54. Husband, B.C. & Schemske, D.W. (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution, 50, 54-70.
55. IUCN (1998) IUCN Guidelines for Reintroductions. Prepared by the IUCN/SSC Reintroductions Specialist Group, IUCN, Gland, Switzerland, and Cambridge, UK.
56. Jacquard, A. (1975) Inbreeding: one word, several meanings. Theoretical Population Biology, 7, 338-363.
57. James, J.W. (1970) The founder effect and response to artificial selection. Genetical Research, 16: 241-250.
58. Jamieson, I.G. (2011) Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conservation Biology, 25, 115-123.
59. Jamieson, I.G. & Lacy, R.C. (2011) Managing genetic issues in reintroduction biology. In Reintroduction Biology: integrating science and management, eds J.G.Ewen, D.P. Armstrong, K.A. Parker&P.J. Seddon, Chapter 13. Wiley-Blackwell, Oxford, UK.
60. Jamieson, I.G., Roy, M.S. & Lettink, M. (2003) Sex-specific consequences of recent inbreeding in an ancestrally inbred population of New Zealand takahe. Conservation Biology, 17, 708-716.
61. Jamieson, I.G., Taylor, S.S., Tracy, L.N. et al. (2009) Why some species of birds do not avoid inbreeding: insights from New Zealand robins and saddlebacks. Behavioral Ecology, 20, 575-584.
62. Jamieson, I.G., Tracy, L.N., Fletcher, D. et al. (2007) Moderate inbreeding depression in a reintroduced population of North Island robins. Animal Conservation, 10, 95-102.
63. Jiménez, J.A., Hughes, K.A., Alaks, G. et al. (1994)Anexperimental-study of inbreeding depression in a natural habitat. Science, 266, 271-273.
64. Johnson, J.A., Talbot, S.L., Sage, G.K. et al. (2010b) The use of genetics for the management of a recovering population: temporal assessment of migratory peregrine falcons in North America. PlosOne, 5 (11), e14042, doi:10.1371/journal.pone.0014042.
65. Joron, M.& Brakefield, P.M. (2003) Captivity masks inbreeding effects on male mating success in butterflies. Nature, 424, 191-194.
66. Kalinowski, S.T. & Hedrick, P.W. (1999) Detecting inbreeding depression is difficult in captive endangered species. Animal Conservation, 2, 131-136.
67. Keller, L.F. (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution, 52, 240-250.
68. Keller, L.F. & Waller, D.M. (2002) Inbreeding effects in wild populations. Trends in Ecology and Evolution, 17, 230-241.
69. Keller, L.F., Biebach, I. & Hoeck, P.E.A. (2007) The need for a better understanding of inbreeding effects on population growth. Animal Conservation, 10, 286-287.
70. Keller, L.F., Grant, P.R., Grant, B.R. et al. (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution, 56, 1229-1239.
71. Keller, L.F., Jeffery, K.J., Arcese, P. et al. (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proceedings of the Royal Society of London B, 268, 1387-1394.
72. Keller, L.F., Marr, A.B. & Reid, J.M. (2006) The genetic consequences of small population size: inbreeding and loss of genetic variation. In Conservation and Biology of Small Populations, eds J.N.M. Smith, L.F. Keller, A.B. Marr & P. Arcese, pp. 113-137. Oxford University Press, New York, USA.
73. Keller, L.F., Reid, J.M. & Arcese, P. (2008) Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows. Proceedings of the Royal Society of London B, 275, 597-604.
74. Kimura, M. (1955) Random genetic drift in multi-allelic locus. Evolution, 9, 419-435.
75. Knight, T. (1799) An account of some experiments on the fecundation of vegetables. Philisophical Transactions of the Royal Society of London, 89, 195-204.
76. Kölreuter, J.G. (1766) Vorlöufige Nachricht von einigen das Geschlecht der Pflanzen betreffenden Versuchen und Beobachtungen. Leipzig, Germany.
77. Kristensen, T.N. & Sørensen, A.C. (2005) Inbreeding-lessons from animal breeding, evolutionary biology and conservation genetics. Animal Science, 80, 121-133.
78. Kristensen, T.N., Barker, J.S.F., Pedersen, K.S. et al. (2008) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and seminatural conditions. Proceedings of the Royal Society of London B, 275, 2055-2061.
79. Kristensen, T.N., Sørensen, A.C., Sørensen, D. et al. (2005) A test of quantitative genetic theory using Drosophila-effects of inbreeding and rate of inbreeding on heritabilities and variance components. Journal of Evolutionary Biology, 18, 763-770.
80. Lacy, R.C. (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conservation Biology, 1, 143-158.
81. Lacy, R.C. (1995) Clarification of genetic terms and their use in the management of captive populations. Zoo Biology, 14, 565-577.
82. Lacy, R.C. & Ballou, J.D. (1998) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution, 52, 900-909.
83. Lacy, R.C., Alaks, G. & Walsh, A. (1996) Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution, 50, 2187-2200.
84. Laikre, L., Nilsson, T., Primmer, C.R. et al. (2009) Importance of genetics in the interpretation of favourable conservation status. Conservation Biology, 23, 1378-1381.
85. Lande, R. (1995) Mutation and conservation. Conservation Biology, 9, 782-791.
86. Lande, R. (1998) Risk of population extinction from fixation of deleterious and reverse mutations. Genetica, 103, 21-27.
87. Lande, R. & Barrowclough, G.F. (1987) Effective population size, genetic variation, and their use in population management. In Viable Populations for Conservation, ed. M.E. Soulé, pp. 87-123. Cambridge University Press, Cambridge, UK.
88. Laws, R.J. & Jamieson, I.G. (2011) Is lack of evidence of inbreeding depression in a threatened New Zealand robin indicative of reduced genetic load? Animal Conservation, 14, 47-55.
89. Leberg, P.L. (1993) Strategies for population reintroduction: effects of genetic variability on population growth and size. Conservation Biology, 7, 194-199.
90. Leberg, P.L. & Firmin, B.D. (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Molecular Ecology, 17, 334-343.
91. Leimu, R. & Mutikainen, P. (2005) Population history, mating system, and fitness variation in a perennial herb with a fragmented distribution. Conservation Biology, 19, 349-356.
92. Lerner, I.M. (1954) Genetic Homeostasis. Oliver and Boyd, Edinburgh, UK.
93. Lynch, M. (1996) A quantitative-genetic perspective on conservation issues. In Conservation Genetics: case histories from nature, eds J.C. Avise & J.L. Hamrick, pp. 471-501. Chapman & Hall, New York, USA.
94. Malécot, G. (1948) Les Mathématiques de l'Hérédité.Masson & Cie, Paris, France.
95. Marr, A.B., Arcese, P., Hochachka, W.M. et al. (2006) Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. Journal of Animal Ecology, 75, 1406-1415.
96. Mikkelsen, K., Loeschcke, V. & Kristensen, T.N. (2010) Trait specific consequences of fast and slow inbreeding: lessons from captive populations of Drosophila melanogaster. Conservation Genetics, 11, 479-488.
97. Miller, P.S. & Hedrick, P.W. (2001) Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. Journal of Evolutionary Biology, 14, 595-601.
98. Moorad, J.A. & Wade, M.J. (2005) A genetic interpretation of the variation in inbreeding depression. Genetics, 170, 1373-1384.
99. Nei, M., Maruyama, T. & Chakraborty, R. (1975) The bottleneck effect and genetic variability in populations. Evolution, 29, 1-10.
100. Nepoux, V., Haag, C.R. & Kawecki, T.J. (2010) Effects of inbreeding on aversive learning in Drosophila. Journal of Evolutionary Biology, 23, 2333-2345.
101. Newman, D. & Pilson, D. (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution, 51, 354-362.
102. O'Ryan, C., Harley, E.H., Bruford, M.W. et al. (1998) Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Animal Conservation, 1, 85-94.
103. Ralls, K., Ballou, J.D. & Templeton, A. (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology, 2, 185-193.
104. Ralls, K., Brugger, K. & Ballou, J. (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science, 206, 1101-1103.
105. Reed, D.H. & Bryant, E.H. (2001) Fitness, genetic load and purging in experimental populations of the housefly. Conservation Genetics, 2, 57-62.
106. Robert, A. (2009) Captive breeding genetics and reintroduction success. Biological Conservation, 142, 2915-2922.
107. Roff, D.A. & Emerson, K. (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution, 60, 1981-1990.
108. Ross-Gillespie, A., O'Riain, M.J. & Keller, L.F. (2007) Viral epizootic reveals inbreeding depression in a habitually inbreeding mammal. Evolution, 61, 2268-2273.
109. Saccheri, I. & Hanski, I. (2006) Natural selection and population dynamics. Trends in Ecology and Evolution, 21, 341-347.
110. Saccheri, I., Kuussaari, M., Kankare, M. et al. (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
111. Schwartz, M.K., Luikart, G. &Waples, R.S. (2007) Genetic monitoring as a promising tool for conservation and management. Trends in Ecology and Evolution, 22, 25-33.
112. Soulé, M.E. (1980) Thresholds for survival: maintaining fitness and evolutionary potential. In Conservation Biology: an evolutionary-ecological perspective, eds M.E. Soulé & B.A. Wilcox, pp. 151-169. Sinauer Associates, Inc., Sunderland, Massachusetts, USA.
113. Swindell, W.R. & Bouzat, J.L. (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. Journal of Evolutionary Biology, 19, 1257-1264.
114. Swinnerton, K.J., Groombridge, J.J., Jones, C.G. et al. (2004) Inbreeding depression and founder diversity among captive and free-living populations of the endangered pink pigeon Columba mayeri. Animal Conservation, 7, 353-364.
115. Szulkin, M. & Sheldon, B.C. (2007) The environmental dependence of inbreeding depression in a wild bird population. PlosOne, 2 (10), e1027, doi: 10.1371/journal.pone.0001027.
116. Szulkin, M., Bierne, N. & David, P. (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution, 64, 1202-1217.
117. Templeton, A. R. (2006) Population Genetics and Microevolutionary Theory.Wiley-Liss, Hoboken, New Jersey, USA.
118. Templeton, A.R. & Read, B. (1984) Factors eliminating inbreeding depression in a captive herd of Speke's gazelle (Gazella spekei). Zoo Biology, 3, 177-199.
119. Thornhill, N.W. (1993) The Natural History of Inbreeding and Outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago, Illinois, USA.
120. van Oosterhout, C., Smith, A.M., Hanfling, B. et al. (2007) The guppy as a conservation model: implications of parasitism and inbreeding for reintroduction success. Conservation Biology, 21, 1573-1583.
121. van Raden, P.M. (1992) Accounting for inbreeding and crossbreeding in genetic evaluation of large populations. Journal of Dairy Science, 75, 3136-3, USA.