Abstract
Conservation genetics studies of populations bottlenecks are commonly framed under the detrimental paradigm of inbreeding depression. This conceptual paradigm presupposes a direct and unambiguous relationship between population size, genetic diversity, fitness, and extinction. Here, I review a series of studies that emphasize the role of chance, selection, and history in determining the genetic consequences of population bottlenecks. The variable responses of bottlenecks to fitness, phenotypic variation, and heritable variation emphasize the necessity to explore the relationship between molecular genetic diversity, fitness, adaptive genetic diversity, and extinction beyond the detrimental paradigm of inbreeding depression. Implications for conservation and management are presented as guidelines and testable predictions regarding the potential effects of bottlenecks on population viability and extinction.
Similar content being viewed by others
References
Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242
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
Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J Hered 88:169–178
Bijlsma R, Bundgaard J, Van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J Evol Biol 12:1125–1137
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
Boakes EH, Wang J, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98:172–182
Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science 134:908–909
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
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
Brewer BA, Lacy RC, Foster ML, Alaks G (1990) Inbreeding depression in insular and central populations of peromyscus mice. J Hered 81:257–266
Brodie ED III (2007) Population size is not genetic quality. Anim Conserv 10:288–290
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
Bryant EH, Meffert LM (1993) The effect of serial founder-flush cycles on quantitative genetic variation in the housefly. Heredity 70:122–129
Bryant EH, Meffert LM (1995) An analysis of selectional response in relation to a population bottleneck. Evolution 49:626–634
Bryant EH, McCommas SA, Combs LM (1986) The effects of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114:1191–1211
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
Carson HL, Wisotzky RG (1989) Increase in genetic variance following a population bottleneck. Am Nat 134:668–673
Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205
Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268
Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796
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
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
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
Crandall KA, Binindaemonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Crnokrak P, Barrett SCH (2002) Purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358
Crnokrak P, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75:530–540
Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270
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
Dahlgaard J, Hoffmann AA (2000) Stress resistance and environmental dependency of inbreeding depression in Drosophila melanogaster. Conserv Biol 14:1187–1192
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
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
DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288–1292
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
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
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
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
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
Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York
Fowler K, Whitlock MC (1999a) The distribution of phenotypic variance with inbreeding. Evolution 53:1143–1156
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
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
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
Frankham R (1995a) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–799
Frankham R (1995b) Conservation genetics. Annu Rev Genet 29:305–327
Frankham R (2005a) Genetics and extinction. Biol Conserv 126:131–140
Frankham R (2005b) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755
Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: effects of purging. Conserv Genet 2:279–285
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
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
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
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
Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454
Groom MJ, Preuninger TE (2000) Population type can influence the magnitude of inbreeding depression in Clarkia concinna (Onagraceae). Evol Ecol 14:155–180
Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) “Ghost” alleles of the Mauritius kestrel. Nature 403:616
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)
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
Haag CR, Sakwinska O, Ebert D (2003) Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57:777–783
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
Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biol 4:719–726
Hansson B, Westerberg L (2008) Heterozygosity-fitness correlations within inbreeding classes: Local or genome-wide effects? Conserv Genet 9:73–83
Hedrick PW (2005) Genetics of populations, 3rd edn. Jones & Bartlett Publishers, Sudbury, MA
Hedrick PW, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet (in press)
Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162
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
Holtsford TP (1996) Variation in inbreeding depression among families and populations of Clarkia tembloriensis (Onagraceae). Heredity 76:83–91
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
Jamieson IG (2007) Role of genetic factors in extinction of island endemics: Complementary or competing explanations? Anim Conserv 10:151–153
Kalinowski ST, Hedrick PW (2001) Inbreeding depression in captive bighorn sheep. Anim Conserv 4:319–324
Kalinowski ST, Hedrick PW, Miller PS (1999) No inbreeding depression observed in Mexican and red wolf captive programs. Conserv Biol 13:1371–1377
Kalinowski ST, Hedrick PW, Miller PS (2000) Inbreeding depression in the speke’s gazelle captive breeding program. Conserv Biol 14:1375–1384
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
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
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
Kirkpatrick M, Jarne P (2000) The effects of a bottleneck on inbreeding depression and the genetic load. Am Nat 155:154–167
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
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
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
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
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
Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V (2009) Research on inbreeding in the ‘omic’ era. Trends Ecol Evol (in press)
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
Lacy RC, Alaks GA, Walsh A (1996) Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution 50:2187–2200
Latta R, Ritland K (1994) The relationship between inbreeding depression and prior inbreeding among populations of four Mimulus taxa. Evolution 48:806–817
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
Lieutenant-Gosselin M, Bernatchez L (2006) Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback. Evolution 60:1658–1668
López-Fanjul C, Villaverde A (1989) Inbreeding increases genetic variance for viability in Drosophila melanogaster. Evolution 43:1800–1804
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA
Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35
Margulis SW (1998) Differential effects of inbreeding at juvenile and adult life-history stages in Peromyscus polionotus. J Mammal 79(1):326–336
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
Miller PS, Hedrick PW (2001) Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J Evol Biol 14:595–601
Moorad JA, Wade MJ (2005) A genetic interpretation of the variation in inbreeding depression. Genetics 170:1373–1384
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
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
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
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
Ouborg NJ, Van Treuren R (1995) Variation in fitness-related characters among small and large populations of salvia pratensis. J Ecol 83:369–380
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
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
Pray LA, Goodnight CJ (1995) Genetic variation in inbreeding depression in the red flour beetle Tribolium castaneum. Evolution 49:176–188
Radwan J (2003) Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90:371–376
Ralls K, Brugger K, Ballou JD (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206:1103
Reed DH (2007) Extinction of island endemics: it is not inbreeding depression. Anim Conserv 10:145–146
Reed DH, Bryant EH (2001) Fitness, genetic load and purging in experimental populations of the housefly. Conserv Genet 2:57–62
Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3:301–307
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
Reed DH, Lowe EH, Briscoe DA, Frankham R (2003b) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4:405–410
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
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
Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the Seychelles warbler: environment-dependent maternal effects. Evolution 58:2037–2048
Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81:28–37
Roff DA (2002) Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution 56:768–775
Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50:2000–2013
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
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
Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas WL (1983) Genetics and conservation. Benjamin/Cummings, Menlo Park, CA
Shaffer M (1981) Minimum population sizes for species conservation. Biosciences 31:131–134
Soulé ME (ed) (1987) Viable populations for conservation. Sinauer, Sunderland, MA
Soulé ME, Wilcox BM (1980) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, MA
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
Swindell WR, Bouzat JL (2005) Modeling the adaptive potential of isolated populations: experimental simulations using Drosophila. Evolution 59:2159–2169
Swindell WR, Bouzat JL (2006a) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19:1257–1264
Swindell WR, Bouzat JL (2006b) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762–767
Swindell WR, Bouzat JL (2006c) Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60:1014–1022
Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496
Thornhill NW (1993) The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago, IL
Turelli M, Barton NH (2006) Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60:1763–1776
Van Buskirk J, Willi Y (2006) The change in quantitative genetic variation with inbreeding. Evolution 60:2428–2434
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
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
Visscher PM, Smith D, Hall SJG, Williams JL (2001) A viable herd of genetically uniform cattle. Nature 409:303
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
Waller DM, Dole J, Bersch AJ (2008) Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution 62:917–931
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
Whitlock MC, Fowler K (1996) The distribution among populations in phenotypic variance with inbreeding. Evolution 50:1919–1926
Willis JH, Orr HA (1993) Increased heritable variation following population bottlenecks: the role of dominance. Evolution 47:949–957
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
Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833–843
Acknowledgements
This paper was presented at the European Science Foundation ConGen Conference: Integrating Population Genetics and Conservation Biology held in Trondheim, Norway, 23–26 May 2009. I would like to thank Volker Loeschcke, Kuke Bijlsma, and Kjetil Hindar for allowing my participation in the conference and the ESF for providing financial support. I would also like to acknowledge Lukas Keller, who brought to my attention the potential chance effects of parameter estimation when moving from individual to population estimates, Kuke Bijlsma who emphasized the differential effects of inbreeding on fitness components, and R.C. Woodruff and two anonymous reviewers who provided helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bouzat, J.L. Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet 11, 463–478 (2010). https://doi.org/10.1007/s10592-010-0049-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0049-0