Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Journal of Evolutionary Biology

Volumn 27, Issue 9, 2014, Pages 1975-1989

  Berger, D ^a,b   Walters, R J ^b,c   Blanckenhorn, W U ^b  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

Adaptation; Canalization; Generalist; Multivariate trade off; Performance curve; Phenotypic plasticity; Reaction norm; Specialist; Temperature tolerance

Indexed keywords

DIPTERA; SCATHOPHAGIDAE; SEPSIDAE; SEPSIS (DIPTERAN FLY); SEPSIS PUNCTUM;

ADAPTATION; ANIMAL; BODY SIZE; DIPTERA; EVOLUTION; FEMALE; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY; REPRODUCTIVE FITNESS; SURVIVAL RATE; TEMPERATURE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; DIPTERA; FEMALE; GENETIC FITNESS; GENETIC VARIATION; PHENOTYPE; SURVIVAL RATE; TEMPERATURE;

EID: 84906794002     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12452     Document Type: Article

References (91)

1. Agrawal, A.F. & Stinchcombe, J.R. 2009. How much do genetic covariances alter the rate of adaptation? Proc. R. Soc. B 276: 1183-1191.
2. Angilletta, M.J. 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press, Oxford.
3. Angilletta, M.J. & Dunham, A.E. 2003. The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am. Nat. 162: 332-342.
4. Angilletta, M.J., Wilson, R.S., Navas, C.A. & James, R.S. 2003. Tradeoffs and the evolution of thermal reaction norms. Trends Ecol. Evol. 18: 234-240.
5. Angilletta, M.J., Huey, R.B. & Frazier, M.R. 2010. Thermodynamic effects on organismal performance: is hotter better? Physiol. Biochem. Zool. 83: 197-206.
6. Atkinson, D. & Sibly, R.M. 1997. Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol. Evol. 12: 235-239.
7. Bates, D., Maechler, M. & Bolker, B. 2011. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4
8. Bell, G. & Gonzales, A. 2009. Evolutionary rescue can prevent extinction following environmental change. Ecol. Lett. 12: 942-948.
9. Bennett, A.F. & Lenski, R.E. 1993. Evolutionary adaptation to temperature II. Thermal niches of experimental lines of Escherichia coli. Evolution 47: 1-12.
10. Bennett, A.F. & Lenski, R.E. 1997. Evolutionary adaptation to temperature. VI. Phenotypic acclimation and its evolution in Escherichia coli. Evolution 51: 36-44.
11. Bennett, A.F. & Lenski, R.E. 2007. An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl. Acad. Sci. USA 104: 8649-8654.
12. Bennett, A.F., Lenski, R.E. & Mittler, J.E. 1992. Evolutionary adaptation to temperature I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46: 16-30.
13. Berger, D., Bauerfeind, S.S., Blanckenhorn, W.U. & Schäfer, M.A. 2011a. High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution 65: 2830-2842.
14. Berger, D., Friberg, M. & Gotthard, K. 2011b. Divergence and ontogenetic coupling of larva behavior and thermal reaction norms in three closely related butterflies. Proc. R. Soc. Lond. B 278: 313-320.
15. Berger, D., Postma, E., Blanckenhorn, W.U. & Walters, R.J. 2013. Quantitative genetic divergence and standing genetic (co)variance in thermal reaction norms along latitude. Evolution 67: 2385-2399.
16. Berger, D., Grieshop, K., Lind, M.I., Goenaga, J., Maklakov, A.A. & Arnqvist, G. 2014. Intralocus sexual conflict and environmental tolerance. Evolution. doi/10.1111/evo.12439.
17. Blanckenhorn, W.U. 2000. The evolution of body size: What keeps organisms small? Q. Rev. Biol. 75: 388-407.
18. Blanckenhorn, W.U., Stillwell, R.C., Young, K.A., Fox, C.W. & Ashton, K.G. 2006. When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution 60: 2004-2011.
19. Blanckenhorn, W.U., Pemberton, A.J., Bussière, L.F., Roembke, J. & Floate, K.D. 2010. Natural history and laboratory culture of the yellow dung fly, Scathophaga stercoraria (L.; Diptera: Scathophagidae). J. Insect Sci. 10: 1-17.
20. Bonduriansky, R. 2007. The evolution of condition-dependent sexual size dimorphism. Am. Nat. 169: 9-19.
21. Callahan, H.S., Maughan, H. & Steiner, U.K. 2008. Phenotypic plasticity, costs of phenotypes, and costs of plasticity. Toward an integrative view. Ann. N.Y. Acad. Sci. 1133: 44-66.
22. Chevin, L., Gallet, R., Gomulkiewicz, R., Holt, R.D. & Fellous, S. 2013. Phenotypic plasticity in evolutionary rescue experiments. Philos. Trans. R. Soc. B 368: 20120089.
23. Clarke, A. 2003. Costs and consequences of evolutionary temperature adaptation. Trends Ecol. Evol. 18: 573-581.
24. Condon, C., Cooper, B.S., Yeaman, S. & Angilletta, M.J. 2013. Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster. Evolution 68: 720-728.
25. Conner, J.K. 2012. Quantitative genetic approaches to evolutionary constraint: how useful? Evolution 66: 3313-3320.
26. Conover, D.O. & Schultz, E.T. 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol. Evol. 10: 248-252.
27. Cooper, B.S., Hammad, L.A., Fisher, N.P., Karty, J.A. & Montooth, K.L. 2012. In a variable thermal environment selection favors greater plasticity of cell membranes in Drosophila melanogaster. Evolution 66: 1976-1984.
28. Crispo, E. 2008. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J. Evol. Biol. 21: 1460-1469.
29. DeWitt, T.J., Sih, A. & Wilson, D.S. 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13: 77-81.
30. Diamond, S.E. & Kingsolver, J.G. 2010. Environmental dependence of thermal reaction norms: host plant quality can reverse the temperature-size rule. Am. Nat. 175: 1-10.
31. Dmitriew, C.M. 2011. The evolution of growth trajectories: what limits growth rate? Biol. Rev. 86: 97-116.
32. Dmitriew, C.M. & Blanckenhorn, W.U. 2012. The role of sexual selection and conflict in mediating among-population variation in mating strategies and sexually dimorphic traits in Sepsis punctum. PLoS ONE 7: e49511.
33. Elena, S.F. & Lenski, R.E. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4: 457-469.
34. Foray, V., Desouhant, E. & Gibert, P. 2014. The impact of thermal fluctuations on reaction norms in specialist and generalist parasitic wasps. Funct. Ecol. 28: 411-423.
35. Fox, C.W. & Mousseau, T.A. 1998. Maternal effects as adaptation for transgenerational phenotypic plasticity in insects. In: Maternal Effects as Adaptations, Ch 10 (T.A. Mousseau & C.W. Fox, eds), pp. 159-177. Oxford University Press, New York.
36. Frazier, M.R., Huey, R.B. & Berrigan, D. 2006. Thermodynamics constrain the evolution of insect population growth rates: 'warmer is better'. Am. Nat. 168: 512-520.
37. Gabriel, W. 2005. How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18: 873-883.
38. Gabriel, W. & Lynch, M. 1992. The selective advantage of reaction norms for environmental tolerance. J. Evol. Biol. 5: 41-59.
39. Ghalambor, C.K., McKay, J.K., Carroll, S.P. & Reznick, D.N. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21: 394-407.
40. Gilchrist, G.W. 1995. Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am. Nat. 146: 252-270.
41. Grether, G.F. 2005. Environmental change, phenotypic plasticity, and genetic compensation. Am. Nat. 166: E115-E123.
42. Hadfield, J.D. 2008. Estimating evolutionary parameters when viability selection is operating. Proc. R. Soc. B 275: 723-734.
43. Hochachka, P.W. & Somero, G.N. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, Oxford.
44. Hoffmann, A.A. 1995. Acclimation: increasing survival at a cost. Trends Ecol. Evol. 10: 1-2.
45. Hoffmann, A.A. 2010. Physiological climatic limits in Drosophila: patterns and implications. J. Exp. Biol. 213: 870-880.
46. Houle, D. 1991. Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45: 630-648.
47. Huey, R.B. & Kingsolver, J.G. 1989. Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4: 131-135.
48. Huey, R.B. & Kingsolver, J.G. 1993. Evolution of resistance to high temperature in ectotherms. Am. Nat. 142: S21-S46.
49. Hughes, B.S., Cullum, A.J. & Bennett, A.F. 2007. An experimental evolutionary study on adaptation to temporally fluctuating pH in Escherichia coli. Physiol. Biochem. Zool. 80: 406-421.
50. Izem, R. & Kingsolver, J.G. 2005. Variation in continuous reaction norms: quantifying directions of biological interest. Am. Nat. 166: 277-289.
51. de Jong, G. & van Noordwijk, A.J. 1992. Acquisition and allocation of resources: genetic (co)variances, selection, and life histories. Am. Nat. 139: 749-770.
52. Kassen, R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15: 173-190.
53. Kassen, R. & Bell, G. 1998. Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time and space. Heredity 80: 732-741.
54. Ketola, T., Kristensen, T.N., Kellermann, V.M. & Loeschcke, V. 2012. Can evolution of sexual dimorphism be triggered by developmental temperatures? J. Evol. Biol. 25: 847-855.
55. Kingsolver, J.G. & Gomulkiewicz, R. 2003. Environmental variation and selection on performance curves. Integr. Comp. Biol. 43: 470-477.
56. Kingsolver, J.G. & Huey, R.B. 2008. Size, temperature, and fitness: three rules. Evol. Ecol. Res. 10: 251-268.
57. Kingsolver, J.G., Massie, K.R., Schlichta, J.G., Smith, M.H., Ragland, G.J. & Gomulkiewicz, R. 2007. Relating environmental variation to selection on reaction norms: and experimental test. Am. Nat. 169: 163-174.
58. Klepsatel, P., Galikova, M., De Maio, N., Huber, C.D., Schlötterer, C. & Flatt, T. 2013. Variation in thermal performance and reaction norms among populations of Drosophila melanogaster. Evolution 67: 3573-3587.
59. Knies, J.L., Kingsolver, J.G. & Burch, C.L. 2009. Hotter is better and broader: thermal sensitivity of fitness in a population of bacteriophages. Am. Nat. 173: 419-430.
60. Lande, R. 2014. Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment. J. Evol. Biol. 27: 866-875.
61. Latimer, C.A.L., Wilson, R.S. & Chenoweth, S.F. 2011. Quantitative genetic variation for thermal performance curves within and among natural populations of Drosophila serrata. J. Evol. Biol. 24: 965-975.
62. Latimer, C.A., McGuigan, K., Wilson, R.S., Blows, M.W. & Chenoweth, S.F. 2014. The contribution of spontaneous mutations to thermal sensitivity curve variation in Drosophila serrata. Evolution 68: 1824-1837.
63. Leroi, A.M., Bennett, A.F. & Lenski, R.E. 1994. Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation hypothesis. Proc. Natl. Acad. Sci. USA 91: 1917-1921.
64. Levins, R. 1968. Evolution in Changing Environments. Princeton University Press, Princeton, NJ.
65. Lynch, M. & Gabriel, W. 1987. Environmental tolerance. Am. Nat. 129: 283-303.
66. Martin, G. & Lenormand, T. 2006. The fitness effect of mutations across environments: a survey in light of fitness landscape models. Evolution 60: 2413-2427.
67. Murren, C.J., Maclean, H.J., Diamond, S.E., Steiner, U.K., Heskel, M.A., Handelsman, C.A. et al. 2014. Evolutionary change in continuous reaction norms. Am. Nat. 183: 453-467.
68. Nilsson-Örtman, V., Stoks, R. & Johansson, F. 2014. Competitive interactions modify the temperature dependence of damselfly growth rates. Ecology 95: 1394-1406.
69. Pigliucci, M. 2005. Evolution of phenotypic plasticity: where are we going? Trends Ecol. Evol. 20: 481-486.
70. Pont, A.C. & Meier, R. 2002. The Sepsidae (Diptera) of Europe. Fauna Ecol. Scand. 37: 1-222.
71. Puniamoorthy, N., Schäfer, M.A. & Blanckenhorn, W.U. 2012a. Sexual selection accounts for the geographic reversal of sexual size dimorphism in the dung fly Sepsis punctum (Diptera: Sepsidae). Evolution 66: 2117-2126.
72. Puniamoorthy, N., Blanckenhorn, W.U. & Schaefer, M.A. 2012b. Differential investment in pre- versus post-copulatory sexual selection reinforces a cross-continental reversal of sexual size dimorphism in Sepsis punctum (Diptera: Sepsidae). J. Evol. Biol. 25: 2253-2263.
73. R Development Core Team. 2011. R Foundation for Statistical Computation. R Development Core Team, Vienna, Austria.
74. Reboud, X. & Bell, G. 1997. Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78: 507-514.
75. Relyea, R.A. 2002. Costs of phenotypic plasticity. Am. Nat. 159: 272-282.
76. Rogell, B., Widegren, W., Hallsson, L., Berger, D., Björklund, M. & Maklakov, A.A. 2013. Sex-dependent evolution of life-history traits following adaptation to climate warming. Funct. Ecol. 28: 469-478.
77. Rowe, L. & Houle, D. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263: 1415-1421.
78. Salinas, S. & Munch, S.B. 2012. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15: 159-163.
79. Scheiner, S.M. 2002. Selection experiments and the study of phenotypic plasticity. J. Evol. Biol. 15: 889-898.
80. Snell- Rodd, E.C., Van Dyken, J.D., Cruickshank, T., Wade, M.J. & Moczek, A.P. 2010. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32: 71-81.
81. Stillwell, R.C., Blanckenhorn, W.U., Teder, T., Davidowitz, G. & Fox, C.W. 2010. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu. Rev. Entomol. 55: 227-245.
82. Sultan, S.E. & Spencer, H.G. 2002. Metapopulation structure favors plasticity over local adaptation. Am. Nat. 160: 271-283.
83. Van Buskirk, J. & Steiner, U.K. 2009. The fitness costs of developmental canalization and plasticity. J. Evol. Biol. 22: 852-860.
84. Van Tienderen, P.H. 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45: 1317-1331.
85. Via, S. & Lande, R. 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505-522.
86. Walsh, B. & Blows, M.W. 2009. Abundant genetic variation + strong selection = multivariate genetic constraints: a geometric view of adaptation. Ann. Rev. Ecol. Evol. Syst. 40: 41-59.
87. Walters, R.J., Blanckenhorn, W.U. & Berger, D. 2012. Forecasting extinction risk of ectotherms under climate warming: an evolutionary perspective. Funct. Ecol. 26: 1324-1338.
88. West- Eberhard, M.J. 2003. Developmental Plasticity and Evolution. Oxford University Press, New York, NY.
89. Whitlock, M.C. 1996. The red queen beats the jack-of-alltrades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148: S65-S77.
90. Woods, H.A. & Harrison, J.F. 2002. Interpreting rejections of the beneficial acclimation hypothesis: when is physiological plasticity adaptive? Evolution 56: 1863-1866.
91. Yamahira, K., Kawajiri, M., Takeshi, K. & Irie, T. 2007. Inter- and intrapopulation variation in thermal reaction norms for growth rate: evolution of latitudinal compensation in ectotherms with a genetic constraint. Evolution 61: 1577-1589.