Inbreeding-stress interactions: Evolutionary and conservation consequences

Annals of the New York Academy of Sciences

Volumn 1256, Issue 1, 2012, Pages 33-48

  Reed, David H ^a   Fox, Charles W ^b   Enders, Laramy S ^c   Kristensen, Torsten N ^d  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

Biodiversity conservation; Environmental stress; Evolution; Inbreeding; Omics

Indexed keywords

ARTICLE; CONSERVATION GENETICS; ENVIRONMENTAL STRESS; EPIGENETICS; GENETIC ASSOCIATION; GENETIC LOAD; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; INBREEDING DEPRESSION; INBREEDING STRESS INTERACTION; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PHYSIOLOGICAL PROCESS; PHYSIOLOGICAL STRESS; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84860990522     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06548.x     Document Type: Article

References (129)

1. Bijlsma, R. et al 2000. Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J. Evol. Biol. 13: 502-514.
2. Cheptou, P.O. & K. Donohue 2011. Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol. 189: 395-407.
3. Frankham, R. 2005. Genetics and extinction. Biol. Conserv. 126: 131-140.
4. Hoffmann, A.A. & P.A. Parsons 1997. Extreme Environmental Change and Evolution. Cambridge. Cambridge University Press.
5. Armbruster, P. & D.H. Reed 2005. Inbreeding depression in benign and stressful environments. Heredity 95: 235-242.
6. Fox, C.W. & D.H. Reed 2011. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65: 246-258.
7. Bijlsma, R. & V. Loeschcke 2005. Environmental stress, adaptation and evolution: an overview. J. Evol. Biol. 18: 744-749.
8. Toohey, B.D. & G.A. Kendrick 2007. Survival of juvenile Ecklonia radiata sporophytes after canopy loss. J. Exp. Mar. Biol. Ecol. 349: 170-182.
9. Karsten, U. et al 2001. Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters. Oecologia 127: 11-20.
10. Liao, W. & D.H. Reed 2009. Inbreeding-environment interactions increase extinction risk. Anim. Conserv. 12: 54-61.
11. Robert, A. 2011. Find the weakest link. A comparison between demographic, genetic and demo-genetic metapopulation extinction times. BMC Evol. Biol. 11: 260.
12. Martin, G. & T. Lenormand 2006. The fitness effect of mutations across environments: a survey in light of fitness landscape models. Evolution 60: 2413-2427.
13. Lewis, D. 1955. Gene interaction, environment and hybrid vigour. Proc. Royal Soc. Lond. B 144: 178-185.
14. Maynard Smith, J. 1956. Acclimatization to high temperatures in inbred and outbred Drosophila subobscura. J. Genet. 54: 497-505.
15. Parsons, P.A. 1959. Genotypic-environmental interactions for various temperatures in Drosophila melanogaster. Genetics 44: 1325-1333.
16. Finlay, K.W. 1963. Adaptation: its measurement and significance in barley breeding. In Proceedings of the 1st International Barley Genetics Symposium. Wageningen, The Netherlands
17. Griffing, B. & J. Langridge 1963. Phenotypic stability of growth in the self-fertilised species Arabidopsis thaliana. Stat. Genet. Plant Breed.: NAS-NRC 982: 368-394.
18. Hull, P. et al 1963. A comparison of the interaction, with types of environment, of pure strains or strain crosses of poultry. Genet. Res. 4: 370-381.
19. Bucio-Alanis, L. 1966. Environmental and genotype-environmental components of variability. Heredity 21: 387-405.
20. Pederson, D.G. 1968. Environmental stress, heterozygote advantage and genotype-environment interaction in Arabidopsis. Heredity 23: 127-138.
21. Jinks, J.L. & K. Mather 1955. Stability in development of heterozygotes and homozygotes. Proc. R. Soc. Lond. B 143: 561-578.
22. Waddington, C.H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
23. Lerner, I.M. 1954. Genetic Homeostasis. Wiley. New York.
24. Windig, J.J. et al 2011. Simultaneous estimation of genotype by environment interaction accounting for discrete and continuous environmental descriptors in Irish dairy cattle. J. Dairy Sci. 94: 3137-3147.
25. Wright, S. 1977. Evolution and the Genetics of Populations, Vol. 3. Experimental Results and Evolutionary Deductions. University of Chicago Press. Chicago.
26. Dudash, M.R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis l (Gentianaceae): a comparison in three environments. Evolution 44: 1129-1139.
27. Armbruster, P. et al 2000. Equivalent inbreeding depression under laboratory and field conditions in a tree-hole-breeding mosquito. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 267: 1939-1945.
28. Jimenez, J.A. et al 1994. An experimental study of inbreeding depression in a natural habitat. Science 266: 271-273.
29. Chen, X.F. 1993. Comparison of inbreeding and outbreeding in hermaphroditic Arianta arbustorum (l) (land snail). Heredity 71: 456-461.
30. Johnston, M.O. 1992. Effects of cross and self-fertilization on progeny fitness in Lobelia cardinalis and L. siphilitica. Evolution 46: 688-702.
31. Crnokrak, P. & D.A. Roff 1999. Inbreeding depression in the wild. Heredity 83: 260-270.
32. Dahlgaard, J. et al 1995. Heat-shock tolerance and inbreeding in Drosophila buzzatii. Heredity 74: 157-163.
33. Dahlgaard, J. & V. Loeschcke 1997. Effects of inbreeding in three life stages of Drosophila buzzatii after embryos were exposed to a high temperature stress. Heredity 78: 410-416.
34. Hauser, T.P. & V. Loeschcke 1996. Drought stress and inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae). Evolution 50: 1119-1126.
35. Bijlsma, R. et al 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol. 12: 1125-1137.
36. Kristensen, T.N. et al 2003. Effects of inbreeding and environmental stress on fitness: using Drosophila buzzatii as a model organism. Conserv. Genet. 4: 453-465.
37. Enders, L.S. & L. Nunney 2012. Seasonal stress drives predictable changes in inbreeding depression in captive field populations of Drosophila melanogaster? In revision.
38. Bijlsma, R. & V. Loeschcke 2012. Genetic erosion impedes adaptive responses to stressful environments. Evol. App. 5: 117-129.
39. Keller, L.F. & D.M. Waller 2002. Inbreeding effects in the wild. Trends Ecol. Evol. 17: 230-241.
40. Lynch, M. & B. Walsh 1998. Genetics and Analysis of Quantitative Traits. Sinauer. Sunderland, MA
41. Yang, H.P. et al 2001. Whole-genome effects of ethyl methanesulfonate-induced mutation on nine quantitative traits in outbred Drosophila melanogaster. Genetics 157: 1257-1265.
42. Agrawal, A.F. & M.C. Whitlock 2010. Environmental duress and epistasis: how does stress affect the strength of selection on new mutations. Trends Ecol. Evol. 25: 450-458.
43. Laffafian, A. et al 2010. Variation in the strength and softness of selection on deleterious mutations. Evolution 64: 3232-3241.
44. Vieira, C. et al 2000. Genotype-environment interaction for quantitative trait loci affecting life span in Drosophila melanogaster. Genetics 154: 213-227.
45. Verhoeven, K.J.F. et al 2008. Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations. Mol. Ecol. 14: 3416-3424.
46. Vermeulen, C.J. & R. Bijlsma 2004a. Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding. Heredity 92: 275-281.
47. Vermeulen, C.J. & R. Bijlsma 2004b. Characterization of conditionally expressed mutants affecting age-specific survival in inbred lines of Drosophila melanogaster: lethal conditions and temperature-sensitive periods. Genetics 167: 1241-1248.
48. Korona, R. 1999. Genetic load of the yeast Saccharomyces cerevisiae under diverse environmental conditions. Evolution 53: 1966-1971.
49. Remold, S.K. & R.E. Lenski 2001. Contribution of individual random mutations to genotype-by-environment interactions in Escherichia coli. Proc. Natl. Acad. Sci. USA 98: 11388-11393.
50. Fry, J.D. & S.L. Heinsohn 2002. Environment dependence of mutational parameters for viability in Drosophila melanogaster. Genetics 161: 1155-1167.
51. Estes, S. et al 2005. Spontaneous mutational correlations for life-history, morphological and behavioral characters in Caenorhabditis elegans. Genetics 170: 645-653.
52. Baer, C.F. 2008. Quantifying the decanalizing effects of spontaneous mutations in Rhabditid nematodes. Am. Nat. 172: 272-281.
53. Fry, J.D. et al 1998. QTL mapping of genotype-environment interaction for fitness in Drosophila melanogaster. Genet. Res. 71: 133-141.
54. Fernandéz, J. & C. López-Fanjul 1996. Spontaneous mutational variances and covariances for fitness-related traits in Drosophila melanogaster. Genetics 143: 829-837.
55. Fry, J.D. 2008. Genotype-environment interactions for fitness in Drosophila. J. Genet. 87: 355-362.
56. Fox, C.W. et al 2011. Inbreeding-environment interactions for fitness: complex relationships between inbreeding depression and temperature stress in a seed-feeding beetle. Evol. Ecol. 25: 25-43.
57. Kondrashov, A.S. & D. Houle 1994. Genotype-environment interactions and the estimation of the genomic mutation rate in Drosophila melanogaster. Proc. R. Soc. Lond. B 258: 221-227.
58. Szafraniec, K. et al 2001. Environmental stress and mutational load in diploid strains of the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 1107-1112.
59. Hillenmeyer, M.E. et al 2008. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320: 362-365.
60. Enders, L.S. & L. Nunney 2010. Sex-specific effects of inbreeding in wild-caught Drosophila melanogaster under benign and stressful conditions. J. Evol. Biol. 23: 2309-2323.
61. Waller, D.M. et al 2008. Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution 62: 917-931.
62. Hughes, K.A. et al 2002. A test of evolutionary theories of aging. Proc. Natl. Acad. Sci. USA 99: 14286-14291.
63. Fox, C.W. et al 2006. The genetic architecture of life span and mortality rates: gender and species differences in inbreeding load of two seed-feeding beetles. Genetics 174: 763-773.
64. Fowler, K. & M.C. Whitlock 1999. The distribution of phenotypic variance with inbreeding. Evolution 53: 1143-1156.
65. Reed, D.H. et al 2003. Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage. Evolution 57: 1822-1828.
66. Auld, J.R. & R.A. Relyea 2010. Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail. Biol. Lett. 6: 222-224.
67. Kristensen, T.N. et al 2011. No inbreeding depression for low temperature developmental acclimation across multiple Drosophila species. Evolution 65: 3195-3201.
68. Crow, J.F. 1958. Some possibilities for measuring selection intensities in man. Hum. Biol. 30: 1-13.
69. Downhower, J.F. et al 1987. Opportunity for selection: an appropriate measure for evaluating variation in the potential for selection? Evolution 41: 1395-1400.
70. Badyaev, A.V. & K.R. Foresman 2004. Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. Am. Nat. 163: 868-879.
71. Kassahn, K.S. et al 2009. Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol. Rev. 84: 277-292.
72. Yeyati, P.L. et al 2007. Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet. 3: 431-447.
73. Rutherford, S.L. & S. Lindquist 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
74. Raser, J.M. & E.K. O'Shea 2005. Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
75. Lopez-Maury, L. et al 2008. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat. Rev. Genet. 9: 583-593.
76. Kristensen, T.N. et al 2011. Slow inbred lines of Drosophila melanogaster express as much inbreeding depression as fast inbred lines under semi-natural conditions. Genetica 4: 441-451.
77. Kristensen, T.N. et al 2002. Inbreeding affects Hsp70 expression in two species of Drosophila even at benign temperatures. Evol. Ecol. Res. 4: 1209-1216.
78. Pedersen, K.S. et al 2005. Effects of inbreeding and rate of inbreeding in Drosophila melanogaster: Hsp70 expression and fitness. J. Evol. Biol. 18: 756-762.
79. Sørensen, J.G. et al 2003. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 6: 1025-1037.
80. Paige, K.N. 2010. The functional genomics of inbreeding depression: a new approach to an old problem. Bioscience 60: 267-277.
81. Kristensen, T.N. et al 2006. Inbreeding by environmental interactions affect gene expression in Drosophila melanogaster. Genetics 173: 1329-1336.
82. Kristensen, T.N. et al 2005. Genome-wide analysis on inbreeding effects on gene expression in Drosophila melanogaster. Genetics 171: 157-167.
83. Ayroles, J.F. et al 2009. A genomewide assessment of inbreeding depression: gene number, function, and mode of action. Conserv. Biol. 23: 920-930.
84. Pedersen, K.S. et al 2010. Proteomic characterization of a temperature-sensitive conditional lethal in Drosophila melanogaster. Heredity 104: 125-134.
85. Kristensen, T.N. et al 2010. Research on inbreeding in the 'omic' era. Trends Ecol. Evol. 25: 44-52.
86. Allendorf, F.W. et al 2010. Genomics and the future of conservation genetics. Nat. Rev. Genet. 11: 697-709.
87. Meuwissen, T. 2007. Genomic selection: marker assisted selection on a genome wide scale. J. Anim. Breed. Genet. 124: 321-322.
88. Sonesson, A.K. et al 2010. Maximising genetic gain whilst controlling rates of genomic inbreeding using genomic optimum contribution selection. In Proceedings of the 9th World Congress on Genetics Applied to Livestock Production, 1-6 August 2010, No 892. Leipzig, Germany
89. Hagenblad, J. et al 2009. Population genomics of the inbred Scandinavian wolf. Mol. Ecol. 18: 1341-1351.
90. Sgrò, C.M. et al 2011. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4: 326-337.
91. Casellas, J. et al 2009. Epistasis for founder-specific inbreeding depression in rabbits. J. Hered. 102: 157-164.
92. Kristensen, T.N. et al 2012. No inbreeding depression for low temperature developmental acclimation across multiple Drosophila species. In press.
93. Frankham, R. 2010. Challenges and opportunities of genetic approaches to biological conservation. Biol. Conserv. 143: 1919-1927.
94. Suorsa, P. et al 2003. Forest management is associated with physiological stress in an old-growth forest passerine. Proc. R. Soc. Lond. B 270: 963-969.
95. Martínez-Mota, R. et al 2007. Effects of forest fragmentation on the physiological stress response of black howler monkeys. Anim. Conserv. 10: 374-379.
96. Berger, S. et al 2007. Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana. Horm. Behav. 52: 653-663.
97. Martin, L.B. et al 2010. The effects of anthropogenic global changes on immune functions and disease resistance. Ann. NY Acad. Sci. 1195: 129-148.
98. Fox, C.W. et al 2008. Experimental purging of the genetic load and its implications for the genetics of inbreeding depression. Evolution 62: 2236-2249.
99. Willi, Y. & A.A. Hoffmann 2009. Demographic factors and genetic variation influence population persistence under environmental change. J. Evol. Biol. 22: 124-133.
100. Bouzat, J.L. 2010. Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv. Genet. 11: 463-478.
101. Ouborg, N.J. et al 2010. Conservation genetics in transition to conservation genomics. Trends Genet 26: 177-187.
102. Reed, D.H. 2010. Albatrosses, eagles, and newts, oh my!: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Anim. Conserv. 13: 448-457.
103. O'Grady, J.J. et al 2006. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133: 42-51.
104. Blomqvist, D. et al 2010. Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population. BMC Evol. Biol. 10: 33.
105. Charpentier, M.J.E. et al 2008. Inbreeding depression in ring-tailed lemurs (Lemur catta): genetic diversity predicts parasitism, immunocompetence, and survivorship. Conserv. Genet. 9: 1605-1615.
106. Reed, D.H. et al 2002. Inbreeding and extinction: the effect of environmental stress and lineage. Conserv. Genet. 3: 301-307.
107. Reed, D.H. 2008. The effects of population size on population viability: from mutation to environmental catastrophes. In Conservation Biology: Evolution in Action. S.P. Carroll & C.W. Fox, Eds.: 16-34. Oxford University Press. New York
108. Mousseau, T.A. & C.W. Fox 1998. The adaptive significance of maternal effects. Trends Ecol. Evol. 13: 403-407.
109. Halpern, B.S. et al 2008. A global map of human impact on marine ecosystems. Science 319: 948-952.
110. Crain, C.M. et al 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11: 1304-1315.
111. Eranen, J.K. et al 2009. Mountain birch under multiple stressors - heavy metal-resistant populations co-resistant to biotic stress but maladapted to abiotic stress. J. Evol.Biol. 22: 840-851.
112. O'Donnell, M. et al 2009. Predicted impact of ocean acidification on a marine invertebrate: elevated CO(2) alters response to thermal stress in sea urchin larvae. Mar. Biol. 156: 439-446.
113. Leberg, P.L. & B.D. Firmin 2008. Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 17: 334-343.
114. Hedrick, P.W. 1994. Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73: 363-372.
115. Wang, J.L. et al 1999. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74: 165-178.
116. Wang, J.L. 2000. Effects of population structures and selection strategies on the purging of inbreeding depression due to deleterious mutations. Genet. Res. Genet. Res. 76: 75-86.
117. Charlesworth, D. & J.H. Willis 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10: 783-796.
118. Agrawal, A.F. & M.C. Whitlock 2010. Environmental duress and epistasis: how does stress affect the strength of selection on new mutations? Trends Ecol. Evol. 25: 450-458.
119. Richardson, D.S. et al 2004. Inbreeding in the Seychelles warbler: environment specific maternal effects. Evolution 58: 2037-2048.
120. Rowe, G. & T.J.C. Beebee 2005. Intraspecific competition disadvantages inbred natterjack toad (Bufo calamita) genotypes over outbred ones in a shared pond environment. J. Anim. Ecol. 74: 71-76.
121. Marr, A.B. et al 2006. Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J. Anim. Ecol. 75: 1406-1415.
122. Szulkin, M. & B. Sheldon 2007. The environmental dependence of inbreeding depression in a wild bird population. PLoS One 2: e1027.
123. Reed, D.H. et al 2007. The genetic quality of individuals directly impacts population dynamics. Anim. Conserv. 10: 275-283.
124. Keller, L.F. et al 2002. Environmental conditions affect the magnitude of inbreeding depression in survival of Darwin's finches. Evolution 56: 1229-1239.
125. Hayes, C.N. et al 2005. Environmental variation influences the magnitude of inbreeding depression in Cucurbita pepo ssp texana (Cucurbitaceae). J. Evol. Biol. 18: 147-155.
126. Weinig, C. et al 2003. Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165: 321-329.
127. Zhong, D. et al 2005. Costly resistance to parasitism: evidence from simultaneous quantitative trait mapping for resistance and fitness in Tribolium castaneum. Genetics 169: 2127-2135.
128. Gardner, K.M. & R.G. Latta 2007. Shared quantitative trait loci underlying the genetic correlation between continuous traits. Mol. Ecol. 16: 4195-4209.
129. Wilson, A.J. et al 2006. Environmental coupling of selection and heritability limits evolution. PLoS Biology 7: 1270-1275.