Conservation genetics of population bottlenecks: The role of chance, selection, and history

Conservation Genetics

Volumn 11, Issue 2, 2010, Pages 463-478

  Bouzat, Juan L ^a  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

Extinction; Fitness; Genetic diversity; Inbreeding depression; Population bottlenecks

Indexed keywords

CONCEPTUAL FRAMEWORK; CONSERVATION GENETICS; EXTINCTION RISK; FITNESS; GENETIC VARIATION; GUIDELINE; INBREEDING DEPRESSION; POPULATION BOTTLENECK; POPULATION SIZE;

EID: 77952091764     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-010-0049-0     Document Type: Article

References (140)

1. Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95: 235-242.
2. Ayroles JF, Hughes KA, Rowe KC, Reedy MM, Rodriguez-Zas SL, Drnevich JM, Caceres CE, Paige KN (2009) A genomewide assessment of inbreeding depression: gene number, function, and mode of action. Conserv Biol 23: 920-930.
3. Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J Hered 88: 169-178.
4. Bijlsma R, Bundgaard J, van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J Evol Biol 12: 1125-1137.
5. Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? Predictions from drosophila. J Evol Biol 13: 502-514.
6. Boakes EH, Wang J, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98: 172-182.
7. Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science 134: 908-909.
8. Bouzat JL, Lewin HA, Paige KN (1998) The ghost of genetic diversity past: historical DNA analysis of the Greater Prairie Chicken. Am Nat 152: 1-6.
9. Bouzat JL, Johnson JA, Toepfer JE, Simpson SA, Esker TL, Westemeier RL (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10: 191-201.
10. Brewer BA, Lacy RC, Foster ML, Alaks G (1990) Inbreeding depression in insular and central populations of peromyscus mice. J Hered 81: 257-266.
11. Brodie ED III (2007) Population size is not genetic quality. Anim Conserv 10: 288-290.
12. Brouwer L, Komdeur J, Richardson DS (2007) Heterozygosity-fitness correlations in a bottlenecked island species: a case study on the Seychelles warbler. Mol Ecol 16: 3134-3144.
13. Bryant EH, Meffert LM (1993) The effect of serial founder-flush cycles on quantitative genetic variation in the housefly. Heredity 70: 122-129.
14. Bryant EH, Meffert LM (1995) An analysis of selectional response in relation to a population bottleneck. Evolution 49: 626-634.
15. Bryant EH, McCommas SA, Combs LM (1986) The effects of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114: 1191-1211.
16. Carr DE, Dudash MR (2003) Recent approaches into the genetic basis of inbreeding depression in plants. Philos Trans R Soc Lond B Biol Sci 358: 1071-1084.
17. Carson HL, Wisotzky RG (1989) Increase in genetic variance following a population bottleneck. Am Nat 134: 668-673.
18. Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10: 195-205.
19. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18: 237-268.
20. Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74: 329-340.
21. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10: 783-796.
22. Charlesworth B, Miyo T, Borthwick H (2007) Selection responses of means and inbreeding depression for female fecundity in Drosophila melanogaster suggest contributions from intermediate-frequency alleles to quantitative trait variation. Genet Res 89: 85-91.
23. Charpentier M, Setchell JM, Prugnolle F, Knapp LA, Wickings EJ, Peignot P, Hossaert-McKey M (2005) Genetic diversity and reproductive success in mandrills (Mandrillus sphinx). Proc Natl Acad Sci USA 102: 16723-16728.
24. Cheverud J, Routman E, Jaquish C, Tardif S, Peterson G, Belfiore N, Forman L (1994) Quantitative and molecular genetic variation in captive cotton-top tamarins (Saguinus oedipus). Conserv Biol 8: 95-105.
25. Crandall KA, Binindaemonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15: 290-295.
26. Crnokrak P, Barrett SCH (2002) Purging the genetic load: a review of the experimental evidence. Evolution 56: 2347-2358.
27. Crnokrak P, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75: 530-540.
28. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83: 260-270.
29. Da Silva A, Luikart G, Yoccoz NG, Cohas A, Allaine D (2006) Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota). Conserv Genet 7: 371-382.
30. Dahlgaard J, Hoffmann AA (2000) Stress resistance and environmental dependency of inbreeding depression in Drosophila melanogaster. Conserv Biol 14: 1187-1192.
31. Day SB, Bryant EH, Meffert LM (2003) The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57: 1314-1324.
32. Demontis D, Pertoldi C, Loeschcke V, Mikkelsen K, Axelsson T, Kristensen TN (2009) Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster. Mol Ecol 18: 4551-4563.
33. DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53: 1288-1292.
34. Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57(3): 638-645.
35. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16: 463-475.
36. Ellmer M, Andersson S (2004) Inbreeding depression in Nigella degenii (Ranunculaceae): fitness components compared with morphological and phenological characters. Int J Plant Sci 165: 1055-1061.
37. Fernández A, Toro MA, López-Fanjul C (1995) The effect of inbreeding on the redistribution of genetic variance of fecundity and viability in Tribolium castaneu. Heredity 75: 376-381.
38. Fernández J, Rodríguez-Ramilo ST, Pérez-Figueroa A, López-Fanjul C, Caballero A (2003) Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster. Evolution 57: 558-565.
39. Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York.
40. Fowler K, Whitlock MC (1999a) The distribution of phenotypic variance with inbreeding. Evolution 53: 1143-1156.
41. Fowler K, Whitlock MC (1999b) The variance in inbreeding depression and the recovery of fitness in bottlenecked populations. Proc R Soc Biol Sci B 266: 2061-2066.
42. Fowler K, Whitlock MC (2002) Environmental stress, inbreeding, and the nature of phenotypic and genetic variance in Drosophila melanogaster. Proc R Soc Biol Sci B 269: 677-683.
43. Fox CW, Scheibly KL, Reed DH (2008) Experimental evolution of the genetic load and its implications for the genetic basis of inbreeding depression. Evolution 62: 2236-2249.
44. Frankham R (1995a) Inbreeding and extinction: a threshold effect. Conserv Biol 9: 792-799.
45. Frankham R (1995b) Conservation genetics. Annu Rev Genet 29: 305-327.
46. Frankham R (2005a) Genetics and extinction. Biol Conserv 126: 131-140.
47. Frankham R (2005b) Stress and adaptation in conservation genetics. J Evol Biol 18: 750-755.
48. Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: effects of purging. Conserv Genet 2: 279-285.
49. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge.
50. Fry JD, Heinsohn SL, Mackay TFC (1998) Heterosis for viability, fecundity and male fertility in Drosophila melanogaster: comparison of mutational and standing variation. Genetics 148: 1171-1188.
51. García N, López-Fanjul C, García-Dorado A (1994) The genetics of viability in Drosophila melanogaster: effects of inbreeding and artificial selection. Evolution 48: 1277-1285.
52. Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, MA.
53. Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441-454.
54. Groom MJ, Preuninger TE (2000) Population type can influence the magnitude of inbreeding depression in Clarkia concinna (Onagraceae). Evol Ecol 14: 155-180.
55. Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) "Ghost" alleles of the Mauritius kestrel. Nature 403: 616.
56. Groombridge JJ, Dawson DA, Burke T, Prys-Jones R, de Brooke ML, Shah, N (2009) Evaluating the demographic history of the Seychelles kestrel (Falco araea): genetic evidence for recovery from a population bottleneck following minimal conservation management. Biol Conserv (in press).
57. Grueber CE, Wallis GP, Jamieson IG (2008) Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species. Mol Ecol 17: 3978-3984.
58. Haag CR, Sakwinska O, Ebert D (2003) Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57: 777-783.
59. Hadly EA, Kohn MH, Leonard JA, Wayne RK (1998) A genetic record of population isolation in pocket gophers during Holocene climatic change. Proc Natl Acad Sci USA 95: 6893-6896.
60. Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biol 4: 719-726.
61. Hansson B, Westerberg L (2008) Heterozygosity-fitness correlations within inbreeding classes: Local or genome-wide effects? Conserv Genet 9: 73-83.
62. Hedrick PW (2005) Genetics of populations, 3rd edn. Jones & Bartlett Publishers, Sudbury, MA.
63. Hedrick PW, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet (in press).
64. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31: 139-162.
65. Hogg JT, Forbes SH, Steele BM, Luikart G (2006) Genetic rescue of an insular population of large mammals. Proc R Soc Biol Sci B 273: 1491-1499.
66. Holtsford TP (1996) Variation in inbreeding depression among families and populations of Clarkia tembloriensis (Onagraceae). Heredity 76: 83-91.
67. Jacobsen F, Nesje M, Bachmann L, Lifjeld JT (2008) Significant genetic admixture after reintroduction of peregrine falcon (Falco peregrinus) in southern Scandinavia. Conserv Genet 9: 581-591.
68. Jamieson IG (2007) Role of genetic factors in extinction of island endemics: Complementary or competing explanations? Anim Conserv 10: 151-153.
69. Kalinowski ST, Hedrick PW (2001) Inbreeding depression in captive bighorn sheep. Anim Conserv 4: 319-324.
70. Kalinowski ST, Hedrick PW, Miller PS (1999) No inbreeding depression observed in Mexican and red wolf captive programs. Conserv Biol 13: 1371-1377.
71. Kalinowski ST, Hedrick PW, Miller PS (2000) Inbreeding depression in the speke's gazelle captive breeding program. Conserv Biol 14: 1375-1384.
72. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17: 230-241.
73. Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution 56: 1229-1239.
74. Keller LF, Reid JM, Arcese P (2008) Testing evolutionary models of senescence in a natural population: age and inbreeding effects on fitness components in song sparrows. Proc R Soc Biol Sci B 275: 597-604.
75. Kirkpatrick M, Jarne P (2000) The effects of a bottleneck on inbreeding depression and the genetic load. Am Nat 155: 154-167.
76. Kristensen TN, Dahlgaard J, Loeschcke V (2003) Effects of inbreeding and environmental stress on fitness-using Drosophila buzzatii as a model organism. Conserv Genet 4: 453-465.
77. Kristensen TN, Sorensen AC, Sorensen D, Pedersen KS, Sorensen JG, Loeschcke V (2005) A test of quantitative genetic theory using Drosophila-effects of inbreeding and rate of inbreeding on heritabilities and variance components. J Evol Biol 18: 763-770.
78. Kristensen TN, Sorensen P, Pedersen KS, Kruhoffer M, Loeschcke V (2006) Inbreeding by environmental interactions affect gene expression in Drosophila melanogaster. Genetics 173: 1329-1336.
79. Kristensen TN, Loeschcke V, Hoffmann AA (2008a) Linking inbreeding effects in captive populations with fitness in the wild: Release of replicated Drosophila melanogaster lines under different temperatures. Conserv Biol 22: 189-199.
80. Kristensen TN, Barker JS, Pedersen KS, Loeschcke V (2008b) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and semi-natural conditions. Proc R Soc Biol Sci B 275: 2055-2061.
81. Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V (2009) Research on inbreeding in the 'omic' era. Trends Ecol Evol (in press).
82. Lacy RC, Ballou JD (1998) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution 52: 900-909.
83. Lacy RC, Alaks GA, Walsh A (1996) Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution 50: 2187-2200.
84. Latta R, Ritland K (1994) The relationship between inbreeding depression and prior inbreeding among populations of four Mimulus taxa. Evolution 48: 806-817.
85. Lesbarreres D, Primmer CR, Laurila A, Merila J (2005) Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol Ecol 14: 311-323.
86. Lieutenant-Gosselin M, Bernatchez L (2006) Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback. Evolution 60: 1658-1668.
87. López-Fanjul C, Villaverde A (1989) Inbreeding increases genetic variance for viability in Drosophila melanogaster. Evolution 43: 1800-1804.
88. Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
89. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
90. Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402: 34-35.
91. Margulis SW (1998) Differential effects of inbreeding at juvenile and adult life-history stages in Peromyscus polionotus. J Mammal 79(1): 326-336.
92. Marr AB, Arcese P, Hochachka WM, Reid JM, Keller LF (2006) Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J Anim Ecol 75: 1406-1415.
93. Miller PS, Hedrick PW (2001) Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J Evol Biol 14: 595-601.
94. Moorad JA, Wade MJ (2005) A genetic interpretation of the variation in inbreeding depression. Genetics 170: 1373-1384.
95. 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.
96. Nielsen EE, Hansen MM, Loeschcke V (1999) Genetic variation in time and space: microsatellite analysis of extinct and extant populations of Atlantic salmon. Evolution 53: 261-268.
97. Nieminen M, Singer MC, Fortelius W, Schöps K, Hanski I (2001) Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am Nat 157: 237-244.
98. O'Grady JJ, Brook BW, Reed DH, Ballou JD, Tonkyn DW, Frankham R (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol Conserv 133: 42-51.
99. Ouborg NJ, van Treuren R (1995) Variation in fitness-related characters among small and large populations of salvia pratensis. J Ecol 83: 369-380.
100. Packer C, Pusey AE, Rowley H, Gilbert DA, Martenson J, O'Brien SJ (1991) Case study of a population bottleneck lions of the Ngorongoro Crater, Tanzania. Conserv Biol 5: 219-230.
101. Pedersen KS, Kristensen TN, Loeschcke V (2005) Effects of inbreeding and rate of inbreeding in Drosophila melanogaster-Hsp70 expression and fitness. J Evol Biol 18: 756-762.
102. Pray LA, Goodnight CJ (1995) Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49: 176-188.
103. Radwan J (2003) Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90: 371-376.
104. Ralls K, Brugger K, Ballou JD (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206: 1103.
105. Reed DH (2007) Extinction of island endemics: it is not inbreeding depression. Anim Conserv 10: 145-146.
106. Reed DH, Bryant EH (2001) Fitness, genetic load and purging in experimental populations of the housefly. Conserv Genet 2: 57-62.
107. Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3: 301-307.
108. Reed DH, Lowe EH, Briscoe DA, Frankham R (2003a) Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage. Evolution 57: 1822-1828.
109. Reed DH, Lowe EH, Briscoe DA, Frankham R (2003b) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4: 405-410.
110. Reid JM, Arcese P, Keller LV (2003) Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects. Proc R Soc Biol Sci B 270: 2151-2157.
111. Reid JM, Arcese P, Keller LF, Elliott KH, Sampson L, Hasselquist D (2007) Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia). Proc R Soc Biol Sci B 274: 697-706.
112. Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the Seychelles warbler: environment-dependent maternal effects. Evolution 58: 2037-2048.
113. Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81: 28-37.
114. Roff DA (2002) Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution 56: 768-775.
115. Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50: 2000-2013.
116. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392: 491-494.
117. Saccheri IJ, Wilson JJ, Nichols RA, Bruford MW, Brakefield PM (1999) Inbreeding of bottlenecked butterfly populations: estimation using the likelihood of changes in marker allele frequencies. Genetics 151: 1053-1063.
118. Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL (1983) Genetics and conservation. Benjamin/Cummings, Menlo Park, CA.
119. Shaffer M (1981) Minimum population sizes for species conservation. Biosciences 31: 131-134.
120. Soulé ME (ed) (1987) Viable populations for conservation. Sinauer, Sunderland, MA.
121. Soulé ME, Wilcox BM (1980) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, MA.
122. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101(42): 15261-15264.
123. Swindell WR, Bouzat JL (2005) Modeling the adaptive potential of isolated populations: experimental simulations using Drosophila. Evolution 59: 2159-2169.
124. Swindell WR, Bouzat JL (2006a) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19: 1257-1264.
125. Swindell WR, Bouzat JL (2006b) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60: 762-767.
126. Swindell WR, Bouzat JL (2006c) Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60: 1014-1022.
127. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19: 489-496.
128. Thornhill NW (1993) The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago, IL.
129. Turelli M, Barton NH (2006) Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60: 1763-1776.
130. van Buskirk J, Willi Y (2006) The change in quantitative genetic variation with inbreeding. Evolution 60: 2428-2434.
131. van Heerwaarden B, Willi Y, Kristensen TN, Hoffmann A (2008) Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest drosophila. Genetics 179: 2135-2146.
132. Vilas C, San Miguel E, Amaro R, García C (2006) Relative contribution of inbreeding depression and eroded adaptive diversify to extinction risk in small populations of shore campion. Conserv Biol 20: 229-238.
133. Visscher PM, Smith D, Hall SJG, Williams JL (2001) A viable herd of genetically uniform cattle. Nature 409: 303.
134. Wade MJ, Shuster SM, Stevens L (1996) Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the Flour Beetle, Tribolium castaneum. Evolution 50: 723-733.
135. Waller DM, Dole J, Bersch AJ (2008) Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution 62: 917-931.
136. Westemeier RL, Brawn JD, Simpson SA, Esker TL, Jansen RW, Walk JW, Kershner EL, Bouzat JL, Paige KN (1998) Tracking the long-term decline and recovery of an isolated population. Science 282: 1695-1698.
137. Whitlock MC, Fowler K (1996) The distribution among populations in phenotypic variance with inbreeding. Evolution 50: 1919-1926.
138. Willis JH, Orr HA (1993) Increased heritable variation following population bottlenecks: the role of dominance. Evolution 47: 949-957.
139. Wisely SM, Buskirk SW, Fleming MA, McDonald DB, Ostrander EA (2002) Genetic diversity and fitness in black-footed ferrets before and during a bottleneck. J Hered 93: 231-237.
140. Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9: 833-843.