Can evolution of sexual dimorphism be triggered by developmental temperatures?

Journal of Evolutionary Biology

Volumn 25, Issue 5, 2012, Pages 847-855

  Ketola, T ^a   Kristensen, T N ^b   Kellermann, V M ^b   Loeschcke, V ^b  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Acclimation; Cycling temperature; Drosophila melanogaster; Environmental variation; Fluctuating temperature; Genetic correlation; Genotype by environment interaction; Heat shock tolerance; Heritability; Nested full sib half sib design; Quantitative genetics; Sex difference; Sexual conflict

Indexed keywords

ACCLIMATION; ADAPTATION; ENVIRONMENTAL CHANGE; FLY; GENETIC ANALYSIS; GENETIC VARIATION; GENOTYPE; HEAT SHOCK; HERITABILITY; HOMOLOGY; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SEX-RELATED DIFFERENCE; SEXUAL CONFLICT; SEXUAL DIMORPHISM; TEMPERATURE EFFECT; TOLERANCE;

ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; INHERITANCE; MALE; PHYSIOLOGY; SEXUAL DEVELOPMENT; TEMPERATURE;

ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; HEAT-SHOCK RESPONSE; INHERITANCE PATTERNS; MALE; SELECTION, GENETIC; SEX CHARACTERISTICS; TEMPERATURE;

DROSOPHILA MELANOGASTER;

EID: 84859443112     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02475.x     Document Type: Article

References (62)

1. Andersen, L.H., Kristensen, T.N., Loeschcke, V., Toft, S. & Mayntz, D. 2010. Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosophila melanogaster. J. Insect. Physiol. 56: 336-340.
2. Badyaev, A. 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol. Evol. 17: 369-378.
3. Blanckenhorn, W. 2002. The consistency of quantitative genetic estimates in field and laboratory in the yellow dung fly. Genetica 114: 171-182.
4. de Boer, I.J.M. & van Arendonk, J.A.M. 1992. Prediction of additive and dominance effects in selected or unselected populations with inbreeding. Theor. Appl. Genet. 84: 451-459.
5. Bozinovic, F., Bastias, D.A., Boher, F., Clavijo-Baguet, S., Estay, S.A. & Angilletta, M.J., Jr 2011. The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Phys. Biochem. Zool. 84: 543-552.
6. Bubliy, O.A. & Loeschcke, V. 2001. High stressful temperature and genetic variation of five quantitative traits in Drosophila melanogaster. Genetica 110: 79-85.
7. Chapman, T., Arnqvist, G., Bangham, J. & Rowe, L. 2003. Sexual conflict. Trends Ecol. Evol. 18: 41-47.
8. Charmantier, A. & Garant, D. 2005. Environmental quality and evolutionary potential: lessons from wild populations. Proc. R. Soc. Lond. B 272: 1415-1425.
9. Cowley, D.E. & Atchley, W.R. 1988. Quantitative genetics of Drosophila melanogaster. II Heritabilities and genetic correlations between sexes for head and thorax traits. Genetics 119: 421-433.
10. Cowley, D.E., Atchley, W.R. & Rutledge, J.J. 1986. Quantitative genetics of Drosophila melanogaster. I. Sexual dimorphism in genetic parameters for wing traits. Genetics 114: 549-566.
11. Cudeck, R. & O'Dell, L.L. 1994. Applications of standard error estimates in unrestricted factor analysis: significance tests for factor loadings and correlations. Psych. Bull. 115: 475-487.
12. DeBlock, M. & Stocks, R. 2003. Adaptive sex-specific life history plasticity to temperature and photoperiod in damselfly. J. Evol. Biol. 16: 986-995.
13. Delcourt, M., Blows, M.W. & Rundle, H.D. 2009. Sexually antagonistic variation for fitness in an ancestral and a novel environment. Proc. R. Soc. Lond. B 276: 2009-2014.
14. Delph, L.F. & Bell, D.L. 2008. A test of the differential-plasticity hypothesis for variation in the degree of sexual dimorphism in Silene latifolia. Evol. Ecol. Res. 10: 61-75.
15. DeWitt, T.J. & Scheiner, S.M. 2004. Phenotypic Plasticity. Functional and Conceptual Approaches. Oxford University Press, Oxford.
16. Drobniak, S.M., Wiejazka, D., Arct, A., Dubiec, A., Gustafsson, L. & Cichon, M. 2010. Sex-specific heritability of cell-mediated immune response in the blue tit nestlings (Cyanistes caeruleus) J. Evol. Biol. 23: 1286-1292.
17. Dubiec, A., Cichon, M. & Deptuch, K. 2006. Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings. Proc. R. Soc. Lond. B 273: 1759-1764.
18. Fairbairn, D.J. 2007. Sexual dimorphism in the water strider, Aquarius remigis: a case study of adaptation in response to sexually antagonistic selection. In: Sex, Size and Gender Roles (D.J. Fairbairn, W.U. Blanckenhorn & T. Székely, eds), pp. 97-105. Oxford University Press, Oxford.
19. Fairbairn, D.J. & Roff, D.A. 2006. The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage. Heredity 97: 319-328.
20. Fairbairn, D.J., Blanckenhorn, W.U. & Székely, T. 2007. Sex, Size and Gender Roles. Oxford University Press, Oxford.
21. Falconer, D.S. & Mackay, T.F.C. 1996. Introduction to Quantitative Genetics, 4th edn. Longman, Harlow.
22. Fox, C.W., Bush, M.L., Roff, D.A. & Walling, W.G. 2004. Evolutionary genetics of lifespan and mortality rates in two populations of the seed beetle, Callosobruchus maculatus. Heredity 92: 170-181.
23. Gibson, J.R., Chippindale, A.K. & Rice, W.R. 2001. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc. R. Soc. Lond. B 269: 499-505.
24. Gilmour, A.R., Gogel, B.J., Cullis, B.R., Welham, S.J. & Thompson, R. 2002. ASReml User Guide Release 1.0. VSN International Ltd., Hemel Hempstead.
25. Hare, K.M., Yeong, C. & Cree, A. 2011. Does gestational temperature or prenatal sex ratio influence development of sexual dimorphism in a viviparous skink? J. Exp. Zool. 315: 215-221.
26. Hendrickx, F., Maelfait, J.-P. & Lens, L. 2008. Effect of metal stress on life history divergence and quantitative genetic architecture in a wolf spider. J. Evol. Biol. 21: 183-193.
27. Hoffmann, A.A. & Merilä, J. 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14: 96-101.
28. Hoffmann, A.A., Sørensen, J.G. & Loeschcke, V. 2003. Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm. Biol. 28: 175-216.
29. Hole, A.R. 2007. A comparison of approaches to estimating confidence intervals for willingness to pay measures. Health Econ. 16: 827-840.
30. Innocenti, P. & Morrow, E.H. 2010. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 8: e1000335.
31. Kleinteich, A. & Schneider, J.M. 2010. Evidence for Rensch's rule in an orb-web spider with moderate sexual size dimorphism. Evol. Ecol. Res. 12: 667-683.
32. Krebs, R.A. & Loeschcke, V. 1994. Effects of exposure to short-term heat stress on fitness components in Drosophila melanogaster. J. Evol. Biol. 7: 39-49.
33. Krebs, R.A. & Loeschcke, V. 1995a. Resistance to thermal stress in adult Drosophila buzzatii: acclimation and variation among populations. Biol. J. Linn. Soc. 56: 505-515.
34. Krebs, R.A. & Loeschcke, V. 1995b. Resistance to thermal stress in preadult Drosophila buzzatii: variation among populations and changes in relative resistance across life stages. Biol. J. Linn. Soc. 56: 517-531.
35. Krinsky, I. & Robb, A.L. 1990. On approximating the statistical properties of elasticities: a correction. Rev. Econ. Stat. 72: 189-190.
36. Kristensen, T.N., Hoffmann, A.A., Overgaard, J., Sørensen, J.G., Hallas, R. & Loeschcke, V. 2008. Cost and benefits of cold acclimation in field released Drosophila. Proc. Natl Acad. Sci. USA 105: 216-221.
37. Lande, R. 1980. Sexual dimorphism, sexual selection and adaptation in polygenic characters. Evolution 34: 292-305.
38. LeGalliard, J.-F., Ferriere, R. & Globert, J. 2005. Juvenile growth and survival under dietary restriction: are males and females equal? Oikos 111: 368-376.
39. Levins, R. 1968. Evolution in Changing Environments. Princeton University Press, Princeton.
40. Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland.
41. Lyons, E.E., Miller, D. & Meagher, T.R. 1994. Evolutionary dynamics of sex ratio and gender dimorphism in Silene latifolia I. Environmental effects. J. Hered. 85: 196-203.
42. Messina, F.J. & Fry, J.D. 2003. Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. J. Evol. Biol. 16: 501-509.
43. Meyer, K. 2009. Factor-analytic models for genotype × environment type problems and structured covariance matrices. Genet. Sel. Evol. 41: 21.
44. Miller, C.W. & Emlen, D.J. 2010. Dynamic effects of oviposition site on offspring sexually selected traits and scaling relationships. Evol. Ecol. 24: 375-390.
45. Mokkonen, M., Kokko, H., Koskela, E., Lehtonen, J., Mappes, T., Martiskainen, H. et al. 2011. Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus. Science 334: 972-974.
46. Morgan, T.J. & Mackay, T.F.C. 2006. Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96: 232-242.
47. Norry, F.M., Sambucetti, P., Scannapieco, A.C., Gomez, F.H. & Loeschcke, V. 2007. X-linked QTL for knockdown resistance to high temperature in Drosophila melanogaster. Insect Mol. Biol. 16: 509-513.
48. Pakkasmaa, S., Merilä, J. & O′Hara, R.B. 2003. Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions. Heredity 91: 117-124.
49. Poissant, J., Wilson, A.J. & Coltman, D.W. 2009. Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations. Evolution 64: 97-107.
50. Puurtinen, M., Ketola, T. & Kotiaho, J.S. 2009. The good-genes and compatible-genes benefits of mate choice. Am. Nat. 174: 741-752.
51. Rice, W.R. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735-742.
52. Roff, D.A. 1997. Evolutionary Quantitative Genetics. Chapmann & Hall, New York.
53. Rosivall, B., Szöllösi, E., Hasselquist, D. & Török, J. 2010. Males are sensitive - sex-dependent effect of rearing conditions on nestling growth. Behav. Ecol. Sociobiol. 64: 1555-1562.
54. Rutherford, S.L. & Lindquist, S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
55. Sarup, P., Sørensen, J.G., Dimitrov, K., Barker, J.S.F. & Loeschcke, V. 2006. Climatic adaptation of Drosophila buzzatii populations in southeast Australia. Heredity 96: 479-486.
56. Sgró, C.M. & Hoffmann, A.A. 2004. Genetic correlations, trade-offs and environmental variation. Heredity 93: 241-248.
57. Simons, A.M. & Roff, D.A. 1996. The effects of variable environment on the genetic correlation structure in a field cricket. Evolution 50: 267-275.
58. Sørensen, J.G., Dahlgaard, J. & Loeschcke, V. 2001. Genetic variation in thermal tolerance among natural populations of Drosophila buzzatii: down regulation of Hsp70 expression and variation in heat stress resistance traits. Funct. Ecol. 15: 289-296.
59. Sørensen, J.G., Norry, F.M., Scannapieco, A.C. & Loeschcke, V. 2005. Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the New World. J. Evol. Biol. 18: 829-837.
60. P. J. Evol. Biol. 21: 647-650.
61. Wilson, A.J., Morrissey, M.B., Adams, M.J., Walling, C.A., Guinness, F.E., Pemberton, J.M. et al. 2011. Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus, J. Evol. Biol. 24: 772-783.
62. Zar, J.H. 1999. Biostatistical Analysis, 4th edn. Prentice Hall, New Jersey.