Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster

Evolution

Volumn 68, Issue 3, 2014, Pages 720-728

  Condon, Catriona ^a,b   Cooper, Brandon S ^c   Yeaman, Sam ^d   Angilletta, Michael J ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c INDIANA UNIVERSITY   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Acclimation; Experimental evolution; Phenotypic plasticity; Specialist generalist trade offs; Thermal adaptation

Indexed keywords

ACCLIMATION; FECUNDITY; FITNESS; FLY; GENERALIST; PHENOTYPIC PLASTICITY; SPECIALIZATION; TEMPERATURE EFFECT; TEMPORAL VARIATION; TRADE-OFF;

DROSOPHILA MELANOGASTER;

ACCLIMATIZATION; ADAPTATION; ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; EXPERIMENTAL EVOLUTION; FERTILITY; GENETIC VARIABILITY; GENETICS; MOLECULAR EVOLUTION; PHENOTYPIC PLASTICITY; PHYSIOLOGY; REPRODUCTIVE FITNESS; SPECIALIST-GENERALIST TRADE-OFFS; TEMPERATURE; TEMPERATURE ACCLIMATIZATION;

ACCLIMATION; EXPERIMENTAL EVOLUTION; PHENOTYPIC PLASTICITY; SPECIALIST-GENERALIST TRADE-OFFS; THERMAL ADAPTATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; FERTILITY; GENETIC FITNESS; GENETIC VARIATION; TEMPERATURE;

EID: 84896719271     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12296     Document Type: Article

References (69)

1. Angilletta, M. J. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford Univ. Press, New York.
2. Angilletta, M. J., R. S. Wilson, C. A. Navas, and R. S. James. 2003. Tradeoffs and the evolution of thermal reaction norms. TREE 18:234-240.
3. Barrett, R. D. H., and D. Schluter. 2008. Adaptation from standing genetic variation. TREE 23:38-44.
4. Bennett, A. F., R. E. Lenski, and J. E. Mittler. 1992. Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46:16-30.
5. Berger, D., E. Postma, W. U. Blanckenhorn, and R. J. Walters. 2013. Quantitative genetic divergence and standing genetic (co)variance in thermal reaction norms along latitude. Evolution 67:2385-2399.
6. Bolker, B., M. Brooks, C. Clark, S. Geange, J. Poulsen, M. Stevens, and J. White. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. TREE 24:127-135.
7. Bubliy, O. A., A. Riihimaa, F. M. Norry, and V. Loeschcke. 2002. Variation in resistance and acclimation to low-temperature stress among three geographical strains of Drosophila melanogaster. J Therm Biol 27:337-344.
8. Bull, J. J., and I.-N. Wang. 2010. Optimality models in the age of experimental evolution and genomics. J. Evol. Biol. 23:1820-1838.
9. Burke, M. K., and M. R. Rose. 2009. Experimental evolution with Drosophila. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296:R1847-R1854.
10. Chippindale, A., M. R. Rose, and T. J. Chu. 1996. Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50:753-766.
11. Cooper, B. S., M. Czarnoleski, and M. J. Angilletta. 2010. Acclimation of thermal physiology in natural populations of Drosophila melanogaster: a test of an optimality model. J. Evol. Biol. 23:2346-2355.
12. Cooper, B. S., L. A. Hammad, N. P. Fisher, J. A. Karty, and K. L. Montooth. 2012a. In a variable thermal environment selection favors greater plasticity of cell membranes in Drosophila melanogaster. Evolution 66:1976-1984.
13. Cooper, B. S., J. M. Tharp II, I. I. Jernberg, and M. J. Angilletta. 2012b. Developmental plasticity of thermal tolerances in temperate and subtropical populations of Drosophila melanogaster. J. Therm. Biol. 37:211-216.
14. Cunningham, S., and J. Read. 2002. Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologia 133:112-119.
15. David, J. R., P. Gibert, H. Legout, G. Pétavy, P. Capy, and B. Moreteau. 2004. Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94:3-12.
16. Deere, J. A., and S. L. Chown. 2006. Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 168:630-644.
17. Draghi, J. A., and M. C. Whitlock. 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66:2891-2902.
18. Duncan, A. B., S. Fellous, E. Quillery, and O. Kaltz. 2011. Adaptation of Paramecium caudatum to variable conditions of temperature stress. Res. Microbiol. 162:939-944.
19. Fangue, N. A., M. Hofmeister, and P. M. Schulte. 2006. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J. Exp. Biol. 209:2859-2872.
20. Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19:207-233.
21. Gabriel, W. 1999. Evolution of reversible plastic responses: inducible defenses and environmental tolerance. Pp. 286-305 in C. D. Harvell and R. Tollrian, eds. The ecology and evolution of inducible defenses. The Ecology and Evolution of Inducible Defenses, Princeton, NJ.
22. Gabriel, W., and M. Lynch. 1992. The selective advantage of reaction norms for environmental tolerance. J. Evol. Biol. 5:41-59.
23. Gabriel, W., B. Luttbeg, A. Sih, and R. Tollrian. 2005. Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am. Nat. 166:339-353.
24. Gavrilets, S., and S. M. Scheiner. 1993. The genetics of phenotypic plasticity. V. Evolution of reaction norm shape. J. Evol. Biol. 6:31-48.
25. Gibbs, A. G. 1999. Laboratory selection for the comparative physiologist. J. Exp. Biol. 202:2709-2718.
26. Gilchrist, G. W. 1995. Specialists and generalists in changing environments.1. Fitness landscapes of thermal sensitivity. Am. Nat. 146:252-270.
27. Gilchrist, G. W. 1996. A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution 50:1560-1572.
28. Gilchrist, G. W. 2000. The evolution of thermal sensitivity in changing environments.in K. B. Storey and J. M. Storey, editors. Cell and molecular responses to stress. Volume 1. Environmental stressors and gene responses. Elsevier Science, Amsterdam.
29. Gomulkiewicz, R., and M. Kirkpatrick. 1992. Quantitative genetics and the evolution of reaction norms. Evolution 46:390-411.
30. Hazel, J. R. 1995. Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?Annu. Rev. Physiol. 57:19-42.
31. Hochachka, P. W., and Somero, G. N. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford Univ. Press, Oxford, U.K.
32. Hoffmann, A. A. 2010. A genetic perspective on insect climate specialists. Aust. J. Entomol. 49:93-103.
33. Hoffmann, A. A., and P. A. Parsons. 1993. Direct and correlated responses to selection for desiccation resistance: a comparison of Drosophila melanogaster and D. simulans. J. Evol. Biol. 6:643-657.
34. Hoffmann, A. A. A., and J. J. Shirriffs. 2002. Geographic variation for wing shape in Drosophila serrata. Evolution 56:1068-1073.
35. Hoffmann, A. A., and M. Watson. 1993. Geographical variation in the acclimation responses of Drosophila to temperature extremes. Am. Nat. 142:S93-S113.
36. Hughes, B. S., A. J. Cullum, and A. F. Bennett. 2007a. Evolutionary adaptation to environmntal pH in experimental lineages of Escherichia coli. Evolution 61:1725-1743.
37. Hughes, B. S., A. J. Cullum, and A. F. Bennett. 2007b. An experimental evolutionary study on adaptation to temporally fluctuating pH in Escherichia coli. Physiol. Biochem. Zool. 80:406-421.
38. Kassen, R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15:173-190.
39. Kassen, R., and G. Bell. 1998. Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity 80:732-741.
40. Kellermann, V. M., B. V. Heerwaarden, A. A. Hoffmann, and C. M. Sgrò. 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60:1104-1108.
41. Ketola, T., L. Mikonranta, J. Zhang, K. Saarinen, A. M. Örmälä, V. P. Friman, J. Mappes, and J. Laakso. 2013. Fluctuating temperature leads to evolution of thermal generalism and preadaptation to novel environments. Evolution 67:2936-2944.
42. Klepsatel, P., M. Gáliková, N. De Maio, C. D. Huber, C. Schlötterer, and T. Flatt. 2013. Variation in thermal performance and reaction norms among populations of Drosophila melanogaster. Evolution 67:3573-3587.
43. Klingenberg C. P. 2008. MorphoJ. Faculty of Life Sciences, University of Manchester, Manchester.
44. Klok, C. J., and S. L. Chown. 2003. Resistance to temperature extremes in sub-Antarctic weevils: interspecific variation, population differentiation and acclimation. Biol. J. Linnean. Soc. 78:401-414.
45. Legros, M., and J. C. Koella. 2010. Experimental evolution of specialization by a microsporidian parasite. BMC Evol. Biol. 10:159-165.
46. Levins, R. 1968. Evolution in changing environments. Princeton Univ. Press, Princeton, NJ.
47. Long, T.A.F., L. Rowe, and A.F. Agrawal. 2013. The effects of selective historu and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster. Am. Nat. 4:532-534.
48. Lynch, M. 2010. Scaling expectations for the time to establishment of complex adaptations. PNAS 107:16577-16582.
49. Lynch, M., and W. Gabriel. 1987. Environmental tolerance. Am. Nat. 129:283-303.
50. McGuigan, K., and M. W. Blows. 2010. Evolvability of individual traits in a multivariate context: partitioning the additive genetic variance into common and specific components. Evolution 67:1899-1911.
51. Palmer, M. E., and M. W. Feldman. 2011. Spatial environmental variation can select for evolvability. Evolution 65:2345-2356.
52. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
53. Reboud, X., and G. Bell. 1997. Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78:507-514.
54. Remold, S. 2012. Understanding specialism when the jack of all trades can be the master of all. Proc. R. Soc. B 279:4861-4869.
55. Rohlf, F. J. 2001. tpsDig. State University of New York, StonyBrook, NY.
56. Rose, M. R., L. N. Vu, S. U. Park, and J. L. Graves Jr. 1992. Selection on stress resistance increases longevity in Drosophila melanogaster. Exp. Gerontol. 27:241-250.
57. Service, P., and M. R. Rose. 1985. Genetic covariation among life-history components: the effect of novel environments. Evolution 39:493-4945.
58. Scheiner, S. M. 1993. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24:35-68.
59. Skaug, H., D. Fournier, and A. Nielsen. 2006. glmmADMB: generalized linear mixed models using AD Model Builder. R package version 0.7.2.12.
60. Stillman, J. 2003. Acclimation capacity underlies susceptibility to climate change. Science 301:65.
61. Van Dyken, J. D., and M. J. Wade. 2010. The genetic signature of conditional expression. Genetics 184:557-570.
62. Van Tienderen, P. H. 1991. Evolution of generalists and specialist in spatially heterogeneous environments. Evolution 45:1317-1331.
63. Via, S. 1993. Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? Am. Nat. 142:352-265.
64. Via, S., and R. Lande. 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505-522.
65. Via, S., R. Gomulkiewicz, G. de Jong, S. M. Scheiner, C. D. Schlichting, and P. H. Van Tienderen. 1995. Adaptive phenotypic plasticity: consensus and controversy. TREE 10:212-217.
66. Weaver, S. C., A. C. Brault, W. Kang, and J. J. Holland. 1999. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 4316-4326.
67. Yang, C.-H., P. Belawat, E. Hafen, L. Y. Jan, and Y.-N. Jan. 2008. Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319:1679-1683.
68. Yeaman, S., Y. Chen, and M. C. Whitlock. 2010. No effect of environmental heterogeneity on the maintenance of genetic variation in wing shape in Drosophila melanogaster. Evolution 64:3398-3408.
69. Zuur, A. F., E. N. Ieno, W. NN, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, NY.