Genetic erosion impedes adaptive responses to stressful environments

Evolutionary Applications

Volumn 5, Issue 2, 2012, Pages 117-129

  Bijlsma, R ^a   Loeschcke, Volker ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Anthropogenic stress; Changing environments; Cost of inbreeding; Genetic drift; Genetic variation; Habitat fragmentation; Inbreeding depression; Population persistence

Indexed keywords

EID: 84857623013     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/j.1752-4571.2011.00214.x     Document Type: Article

References (132)

1. Allendorf, F. W., P. A. Hohenlohe, and G. Luikart. 2010. Genomics and the future of conservation genetics. Nature Reviews Genetics 11:697-709.
2. Armbuster, P., and D. H. Reed. 2005. Inbreeding depression in benign and stressful environments. Heredity 95:235-242.
3. Auld, J. R., and R. A. Relyea. 2010. Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail. Biology Letters 6:222-224.
4. Auld, J. R., A. A. Agrawal, and R. A. Relyea. 2010. Re-evaluating the costs and limits of phenotypic plasticity. Proceedings of the Royal Society London B 227:503-511.
5. Bakker, J., M. E. C. van Rijswijk, F. J. Weissing, and R. Bijlsma. 2010. Consequences of fragmentation for the ability to adapt to novel environments in experimental Drosophila metapopulations. Conservation Genetics 11:449-462.
6. Barton, N. H., and M. Turelli. 2004. Effects of genetic drift on variance components under a general model of epistasis. Evolution 28:2111-2132.
7. Beldade, P., A. A. Mateus, and R. A. Keller. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology 20:1347-1363.
8. Bell, G., and A. Gonzalez. 2009. Evolutionary rescue can prevent extinction following environmental change. Ecology Letters 12:942-948.
9. Bell, G., and A. Gonzalez. 2011. Adaptation and evolutionary rescue in metapopulations experiencing environmental deterioration. Science 332:1327-1330.
10. Biebach, I., and L. F. Keller. 2010. Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Conservation Genetics 11:527-538.
11. Bijlsma, R., J. Bundgaard, and W. F. van Putten. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology 12:1125-1137.
12. Bijlsma, R., J. Bundgaard, and A. C. Boerema. 2000. Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila. Journal of Evolutionary Biology 13:502-514.
13. Bijlsma, R., M. D. D. Westerhof, L. P. Roekx, and I. Pen. 2010. Dynamics of genetic rescue in inbred Drosophila melanogaster populations. Conservation Genetics 11:435-448.
14. Bishop, J., and L. Cook. 1981. Genetic Consequences of Man-Made Change. Academic Press, London.
15. Blows, M. W., and A. A. Hoffmann. 2005. A reassessment of genetic limits to evolutionary change. Ecology 86:1371-1384.
16. Bradshaw, A. D. 1965. Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13:115-155.
17. Bradshaw, W. E., and C. M. Holzapfel. 2006. Climate change - Evolutionary response to rapid climate change. Science 312:1477-1478.
18. Bradshaw, A. D., and T. McNeilly. 1991. Evolutionary response to global climate change. Annals of Botany 67(Suppl):5-14.
19. Bridle, J. R., J. Polechova, M. Kawata, and R. K. Butler. 2010. Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecology Letters 13:485-494.
20. Bryant, E. H., S. A. McCommas, and L. M. Combs. 1986. The effect of an experimental bottleneck upon quantitative genetic variance in the housefly. Genetics 114:1191-1211.
21. Bürger, R., and M. Lynch. 1995. Evolution and extinction in a changing environment: a quantitative genetic analysis. Evolution 49:151-163.
22. Carson, R. L. 1962. Silent Spring. Houghton Mifflin, Boston.
23. Charlesworth, B., and D. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18:237-268.
24. Charlesworth, D., and J. H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews Genetics 10:783-796.
25. Cheptou, P.-O., and K. Donohue. 2011. Environment-depend inbreeding depression: its ecological and evolutionary significance. New Phytologyst 189:395-407.
26. Cheptou, P.-O., E. Imbert, J. Lepart, and J. Escarre. 2000. Effects of competition on lifetime estimates of inbreeding depression in the outcrossing plant Crepis sancta (Asteraceae). Journal of Evolutionary Biology 13:522-531.
27. Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. Plos Biology 8:e1000357.
28. Chown, S. L., A. A. Hoffmann, T. N. Kristensen, M. J. Angilletta Jr, N. C. Stenseth, and C. Pertoldi. 2010. Adapting to climate change: a perspective from evolutionary physiology. Climate Research 43:3-15.
29. Crnokrak, P., and D. A. Roff. 1999. Inbreeding depression in the wild. Heredity 83:260-270.
30. Dahlgaard, J., and A. A. Hoffmann. 2000. Stress resistance and environmental dependency of inbreeding depression in Drosophila melanogaster. Conservation Biology 14:1187-1192.
31. Dahlgaard, J., E. Hasson, and V. Loeschcke. 2001. Behavioral differentiation in oviposition activity in Drosophila buzzatii from highland and lowland populations in Argentina: plasticity or thermal adaptation? Evolution 55:738-747.
32. Day, S. B., E. H. Bryant, and L. M. Meffert. 2003. The influence of variable rates of inbreeding on fitness, environmental responsiveness, and evolutionary potential. Evolution 57:1314-1324.
33. DeRose, M. A., and D. A. Roff. 1999. A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288-1929.
34. DiBattista, J. D. 2008. Patterns of genetic variation in anthropogenically impacted populations. Conservation Genetics 9:141-156.
35. Dobzhansky, Th., O. Pavlovsky, B. Spassky, and N. Spassky. 1955. Genetics of natural populations. XXIII. Biological role of deleterious recessives in populations of Drosophila. Genetics 40:781-796.
36. Edmands, S. 2007. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16:463-475.
37. Edmands, S., H. V. Feaman, J. S. Harrison, and C. C. Timmerman. 2005. Genetic consequences of many generations of hybridization between divergent copepod populations. Journal of Heredity 96:114-123.
38. Erickson, D. L., and C. B. Fenster. 2006. Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasiculata. Evolution 60:225-233.
39. Fischer, M., M. van Kleunen, and B. Schmid. 2000. Genetic Allee effects on performance, plasticity and developmental stability in a clonal plant. Ecology Letters 3:530-539.
40. Fox, C. W., and D. H. Reed. 2011. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246-258.
41. Frankham, R. 1995. Effective population size - adult population size ratio's in the wild. Genetical Research 66:95-107.
42. Frankham, R., K. Lees, M. E. Mongomery, P. R. England, E. H. Lowe, and D. A. Brisco. 1999. Do population size bottlenecks reduce evolutionary potential? Animal Conservation 2:255-260.
43. Frankham, R., J. D. Ballou, and D. A. Brisco. 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge.
44. Frankham, R., J. D. Ballou, M. B. D. Eldridge, R. C. Lacy, K. Ralls, M. R. Dudash, and C. B. Fenster. 2011. Predicting the probability of outbreeding depression. Conservation Biology 25:465-475.
45. Franks, S. J., S. Sim, and A. E. Weis. 2007. Rapid evolution of flowering time by an annual plant in response to climate fluctuations. Proceedings of the National Academy of Sciences of the United states of America 104:1278-1282.
46. Garant, D., S. E. Forde, and A. P. Hendry. 2007. The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 21:434-443.
47. Ghalambor, C. K., J. K. McKay, S. P. Carrol, and D. N. Reznick. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptations in new environments. Functional Ecology 21:394-407.
48. Gienapp, P., C. Teplitsky, J. S. Alho, J. A. Mills, and J. Merilä. 2008. Climate change and Evolution: disentangling environmental and genetic responses. Molecular Ecology 17:167-178.
49. Gilligan, D. M., D. A. Briscoe, and R. Frankham. 2005. Comparative losses of quantitative and molecular variation in finite populations of Drosophila melanogaster. Genetical Research 85:47-55.
50. Gomulkiewicz, R., and R. D. Holt. 1995. When does evolution by natural selection prevent extinction? Evolution 49:201-207.
51. Grether, G. F. 2005. Environmental change, phenotypic plasticity, and genetic compensation. American Naturalist 166:E115-E123.
52. Haag, C. R., J. W. Hottinger, M. Riek, and D. Ebert. 2002. Strong inbreeding depression in a Daphnia metapopulation. Evolution 56:518-526.
53. Haldane, J. B. S. 1957. The cost of natural selection. Journal of Genetics 55:511-524.
54. Hedrick, P. W. 1994. Purging inbreeding depression and the probability of extinction - full-sib mating. Heredity 73:363-372.
55. Hedrick, P. W. 2001. Conservation genetics: where are we now? Trends in Ecology and Evolution 16:629-636.
56. Hedrick, P. W., and R. Fredrickson. 2010. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conservation Genetics 11:615-625.
57. Hedrick, P. W., and S. T. Kalinowski. 2000. Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics 31:139-162.
58. Hitch, A. T., and P. L. Leberg. 2006. Breeding distributions of North American bird species moving north as a result of climate change. Conservation Biology 21:534-539.
59. Hoeck, P. A., J. L. Bollmer, P. G. Parker, and L. F. Keller. 2010. Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mocking bird populations (Mimus ssp.). Philosophical Transaction of the Royal Society B 365:1127-1138.
60. Howard, D. J. 1993. Small populations, inbreeding, and speciation. In N. W. Thornhill, ed. The Natural History of Inbreeding and Outbreeding, pp. 118-142. University of Chicago Press, Chicago.
61. Huey, R. B., D. Berrigan, G. W. Gilchrist, and J. C. Herron. 1999. Testing the adaptive significance of acclimation: a strong inference approach. American Zoologist 39:323-336.
62. Jiménez, J. A., K. A. Hughes, G. Alaks, L. Graham, and R. C. Lacy. 1994. An experimental study of inbreeding depression in a natural habitat. Science 266:271-273.
63. Johnson, J. A., M. R. Bellinger, J. E. Toepfer, and P. Dunn. 2004. Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Molecular Ecology 13:2617-2630.
64. Joubert, D., and R. Bijlsma. 2010. Interplay between habitat fragmentation and climate change: inbreeding affects the response to thermal stress in Drosophila melanogaster. Climate Research 43:57-70.
65. Keller, L. F. 1998. Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240-250.
66. Keller, L. F., and D. M. Waller. 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17:230-241.
67. Keller, L. F., P. R. Grant, B. R. Grant, and K. Petren. 2002. Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution 55:937-942.
68. Kellerman, V. K., B. van Heerwaarden, A. A. Hoffmann, and C. Sgró. 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60:1104-1108.
69. Ketola, T., and J. S. Kotiaho. 2009. Inbreeding, energy use and condition. Journal of Evolutionary Biology 22:770-781.
70. Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge.
71. Koelewijn, H. P. 1998. Effects of different levels of inbreeding on progeny fitness in Plantago coronopus. Evolution 52:692-702.
72. Kristensen, T. N., and A. C. Sørensen. 2005. Inbreeding - lessons from animal breeding, evolutionary biology and conservation genetics. Animal Science 80:121-133.
73. Kristensen, T. N., A. C. Sørensen, D. Sorensen, K. S. Pedersen, J. G. Sørensen, and V. Loeschcke. 2005. A test of quantitative genetics theory using Drosophila- effects of inbreeding and the rate of inbreeding on heritabilities and variance components. Journal of Evolutionary Biology 18:736-770.
74. Kristensen, T. N., J. S. F. Barker, K. S. Pedersen, and V. Loeschcke. 2008. Extreme temperatures increase the deleterious consequences of inbreeding under both laboratory and semi-natural conditions. Proceedings of the Royal Society London B 275:2055-2061.
75. Kristensen, T. N., K. S. Pedersen, C. J. Vermeulen, and V. Loeschcke. 2010. Research on inbreeding in the "omics" era. Trends in Ecology and Evolution 25:44-52.
76. Kristensen, T. N., V. Loeschcke, T. Bilde, A. A. Hoffmann, C. Sgró, K. Noreikiene., M. Ondrésik et al. 2011. No inbreeding depression for developmental temperature acclimation across multiple Drosophila species. Evolution 65:3195-3201.
77. Lande, R. 1993. Risk of population extinction from demographic and environmental stochasticity and random catastrophes. American Naturalist 142:911-927.
78. Lande, R. 1995. Mutation and conservation. Conservation Biology 9:782-791.
79. Leimu, R., P. Vergeer, F. Angeloni, and N. J. Ouborg. 2010. Habitat fragmentation, climate change, and inbreeding in plants. Annals of the New York Academy of Sciences 1195:84-98.
80. Lenormand, T. 2002. Gene flow and the limits of natural selection. Trends in ecology and Evolution 17:183-189.
81. Liberg, O., H. Andrén, H.-C. Pederson, D. Sejberg, P. Wabakken, M. Åkesson, and S. Bensch. 2005. Severe inbreeding depression in a wild wolf (Canis lupus) population. Biology Letters 1:17-20.
82. Luikart, G., N. Ryman, D. A. Tallmon, M. K. Schwartz, and F. W. Allendorf. 2010. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics 11:355-373.
83. Luquet, E., J.-P. Léna, P. David, P. Joly, T. Lengagne, N. Perrin, and S. Plénet. 2011. Consequences of genetic erosion on fitness and phenotypic plasticity in European tree frog populations (Hyla aborea). Journal of Evolutionary Biology 24:99-110.
84. Lynch, M., and R. Lande. 1993. Evolution and extinction in response to environmental change. In P. M. Kareiva, J. G. Kingsolver, and R. B. Huey, eds. Biotic Interactions and Global Change, pp. 234-250. Sinauer, Sunderland, MA.
85. MacNair, M. R. 1997. The evolution of plants in metal-contaminated environments. In R. Bijlsma, and V. Loeschcke, eds. Environmental Stress, Adaptation, and Evolution, pp. 3-24. Birkhauser Verlag, Basel.
86. Madsen, T., R. Shine, M. Olsson, and H. Wittzell. 1999. Restoration of an inbred adder population. Nature 402:34-35.
87. Malcom, J. W. 2011. Smaller, scale-free gene networks increase quantitative trait heritability and result in faster population recovery. PLoS ONE 6:14645.
88. Maynard Smith, J. 1989. The causes of extinction. Philosophical Transaction of the Royal Society B 325:241-252.
89. Maynard Smith, J., J. M. Clarke, and M. J. Hollingsworth. 1955. The expression of hybrid vigour in Drosophila subobscura. Proceedings of the Royal Society London B 144:159-171.
90. McKenzie, J. A., and P. Batterham. 1998. Predicting insecticide resistance: mutagenesis, selection and response. Philosophical Transactions Royal Society B 353:1729-1734.
91. Nussey, D. H., A. J. Wilson, and J. F. Brommer. 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology 20:831-844.
92. Orr, H. A., and R. L. Unckless. 2008. Population extinction and the genetics of adaptation. American Naturalist 172:160-169.
93. Ouborg, N. J., C. Pertoldi, V. Loeschcke, R. Bijlsma, and P. W. Hedrick. 2010. Conservation genetics in transition to conservation genomics. Trends in Genetics 26:177-187.
94. Palstra, F. P., and D. E. Ruzzante. 2008. Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology 17:3428-3447.
95. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology and Systematics 37:637-669.
96. Parmesan, C., and G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42.
97. Paschke, M., G. Bernasconi, and B. Schmid. 2003. Population size and identity influence the reaction norm of the rare, endemic plant Cochlearia bavaria across a gradient of environmental stress. Evolution 57:496-508.
98. Pedersen, L. D., A. R. Pedersen, R. Bijlsma, and J. Bundgaard. 2011. The effects of inbreeding and heat stress on male sterility in Drosophila melanogaster. Biological Journal of the Linnean Society 104:432-442.
99. Pemberton, J. 2004. Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology and Evolution 19:613-615.
100. Pertoldi, C., R. Bijlsma, and V. Loeschcke. 2007. Conservation genetics in a globally changing environment: present problems, paradoxes and future challenges. Biodiversity Conservation 16:4147-4163.
101. Pigliucci, M. 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology and Evolution 20:482-486.
102. Pluess, A. R., and J. Stöcklin. 2004. Genetic diversity and fitness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conservation Genetics 5:145-156.
103. Ralls, K., J. D. Ballou, and A. R. Templeton. 1988. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology 2:185-193.
104. Rattner, B. A. 2009. History of wildlife toxicology. Ecotoxicology 18:773-783.
105. Reed, D. H. 2005. Relationship between population size and fitness. Conservation Biology 19:563-568.
106. Reusch, T., and T. Wood. 2007. Molecular ecology of global change. Molecular Ecology 16:3973-3992.
107. Roberts, D. R., and R. G. Andre. 1994. Insecticide resistance issues in vector-borne disease control. American Journal of Tropical Medicine and Hygiene 50(6 Suppl):21-36.
108. Ross-Gillespie, A., M. J. O'Riain, and L. F. Keller. 2007. Viral epizootic reveals inbreeding depression in a habitually inbreeding mammal. Evolution 61:2268-2273.
109. Sacheri, I. J., R. A. Nichols, and P. M. Brakefield. 2001. Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana. Genetical Research Cambridge 77:167-181.
110. Schiegg, K., G. Pasinelli, J. R. Walters, and S. J. Daniels. 2002. Inbreeding and experience affect response to climate change by endangered woodpeckers. Proceedings of the Royal Society London B 269:1153-1159.
111. Schlichting, C. D. 1986. The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17:667-693.
112. Schlichting, C. D., and D. A. Levin. 1986. Effects of inbreeding on phenotypic plasticity in cultivated Phlox. Theoretical and Applied Genetics 72:114-119.
113. Segelbacher, G., S. A. Cushman, B. K. Epperson, M.-J. Fortin, O. Francois, O. J. Hardy, R. Holderegger et al. 2010. Applications of landscape genetics in conservation biology: concepts and challenges. Conservation Genetics 11:375-385.
114. Sgrò, C. M., A. J. Lowe, and A. A. Hoffmann. 2011. Building evolutionary resilience for conserving biodiversity under climate change. Evolutionary Applications 4:326-337.
115. Swindell, W. R., and J. L. Bouzat. 2005. Modelling the adaptive potential of isolated populations: experimental simulations using Drosophila. Evolution 59:2159-2169.
116. Teotónio, H., I. M. Chelo, M. Bradić, M. R. Rose, and A. D. Long. 2009. Experimental evolution reveals natural selection on standing genetic variation. Nature Genetics 41:251-257.
117. Thomas, C. D., A. Cameron, R. E. Green, M. Bakkenes, L. J. Beaumont, Y. C. Collinham, B. F. N. Erasmus et al. 2004. Extinction risks from climate change. Nature 427:145-148.
118. Van Buskirk, J., and Y. Willi. 2006. The change in quantitative genetic variation with inbreeding. Evolution 60:2428-2434.
119. Vermeulen, C. J., and R. Bijlsma. 2004a. Changes in mortality patterns and temperature-dependence of life span in Drosophila melanogaster caused by inbreeding. Heredity 92:275-281.
120. Vermeulen, C. J., and R. Bijlsma. 2004b. Characterization of conditionally expressed mutants effecting age-specific survival in inbred lines of Drosophila melanogaster: lethal conditions and temperature sensitive period. Genetics 167:1241-1248.
121. Vilà, C., A.-K. Sundqvist, Ø. Flagstad, J. Seddon, S. Bjørnerfeldt, I. Kojola, A. Casulli et al. 2003. Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society London B 270:91-97.
122. Vitalis, R., K. Dawson, and P. Boursot. 2001. Interpretation of variation across marker loci as evidence of selection. Genetics 158:1811-1823.
123. Wade, M. J., S. M. Schuster, and L. Stevens. 1996. Inbreeding: its effects on the response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Theoretical Population Biology 25:138-139.
124. Waller, D. M., J. Dole, and A. J. Bersch. 2008. Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution 62:917-931.
125. Westemeier, R. L., J. D. Brawn, S. A. Simpson, T. L. Esker, R. W. Jansen, J. W. Walk, E. L. Kershmer et al. 1998. Tracking the long-term decline and recovery of an isolated population. Science 282:1695-1698.
126. Whitlock, M. C., and K. Fowler. 1999. The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152:345-353.
127. Wilkinson, D. 2001. Is local provenance important in habitat creation? Journal of Applied Ecology 38:1371-1373.
128. Willi, Y., and A. A. Hoffmann. 2009. Demographic factors and genetic variation influence population persistence under environmental change. Journal of Evolutionary Biology 22:124-133.
129. Willi, Y., J. Van Buskirk, and A. A. Hoffmann. 2006. Limits to the adaptive potential of small populations. Annual Review of Ecology and Systematics 37:433-458.
130. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159.
131. Wright, S. 1951. The genetical structure of populations. Annals of Eugenics 15:323-354.
132. Wright, L. I., T. Tregenza, and D. J. Hosken. 2008. Inbreeding, inbreeding depression and extinction. Conservation Genetics 9:833-843.