Genotype-by-environment interactions underlie the expression of pre- and post-copulatory sexually selected traits in guppies

Journal of Evolutionary Biology

Volumn 28, Issue 4, 2015, Pages 959-972

  Evans, J P ^a   Rahman, M M ^a   Gasparini, C ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Condition dependence; Genetic variance; Reaction norm; Sperm quality

Indexed keywords

COPULATION; CYPRINID; FITNESS; FRESHWATER ECOSYSTEM; GENE EXPRESSION; GENOTYPE-ENVIRONMENT INTERACTION; LIFE HISTORY TRAIT; SEXUAL DIMORPHISM; SEXUAL SELECTION; SPERM;

POECILIA RETICULATA;

ANIMAL; COPULATION; FEMALE; GENETIC VARIABILITY; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; MALE; PHYSIOLOGY; POECILIA; QUANTITATIVE TRAIT; SEXUAL BEHAVIOR; SPERMATOZOON;

ANIMALS; COPULATION; FEMALE; GENE-ENVIRONMENT INTERACTION; GENETIC VARIATION; MALE; POECILIA; QUANTITATIVE TRAIT, HERITABLE; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA;

EID: 84928027967     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12627     Document Type: Article

References (82)

1. Åkesson, M., Bensch, S., Hasselquist, D., Tarka, M. & Hansson, B. 2008. Estimating heritabilities and genetic correlations: comparing the 'animal model' with parent-offspring regression using data from a natural population. PLoS ONE 3: e1739.
2. Barber, I., Arnott, S.A., Braithwaite, V.A., Andrew, J. & Huntingford, F.A. 2001. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc. R. Soc. Lond. B 268: 71-76.
3. Bates, D., Maechler, M., Bolker, B.M. & Walker, S. 2014. Linear mixed-effects models using Eigen and S4.
4. Billard, R. & Cosson, M.P. (1990) The energetics of fish sperm motility. In: Controls of Sperm Motility: Biological and Clinical Aspects. (C. Gagnon, ed), pp. 153-173. CRC Press Inc., Boca Raton.
5. Bonduriansky, R. & Rowe, L. 2005. Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae). Evolution 59: 138-151.
6. Boschetto, C., Gasparini, C. & Pilastro, A. 2011. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65: 813-821.
7. Bozynski, C.C. & Liley, N.R. 2003. The effect of female presence on spermiation, and of male sexual activity on 'ready' sperm in the male guppy. Anim. Behav. 65: 53-58.
8. Brooks, R. 2002. Variation in female mate choice within guppy populations: population divergence, multiple ornaments and the maintenance of polymorphism. Genetica 116: 343-358.
9. Brooks, R. & Endler, J.A. 2001. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55: 1002-1015.
10. Browne, W.J., Subramanian, S.V., Jones, K. & Goldstein, H. 2005. Variance partitioning in multilevel logistic models that exhibit overdispersion. J. R. Stat. Soc. A 168: 599-613.
11. Bussiere, L.F., Hunt, J., Stoelting, K.N., Jennions, M.D. & Brooks, R. 2008. Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica 134: 69-78.
12. Carreira, P.V., Imberti, M.A., Mensch, J. & Jose Fanara, J. 2013. Gene-by-Temperature Interactions and Candidate Plasticity Genes for Morphological Traits in Drosophila melanogaster. PLoS ONE 8: e70851.
13. Conner, J.K. & Hartl, D.L. 2004. A Primer of Ecological Genetics. Sinauer Associates Inc, Sunderland, MA.
14. Cotton, S., Fowler, K. & Pomiankowski, A. 2004. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. Lond. B 271: 771-783.
15. Cotton, S., Small, J. & Pomiankowski, A. 2006. Sexual selection and condition-dependent mate preferences. Curr. Biol. 16: R755-R765.
16. Danielson-Francois, A.M., Zhou, Y. & Greenfield, M.D. 2009. Indirect genetic effects and the lek paradox: inter-genotypic competition may strengthen genotype x environment interactions and conserve genetic variance. Genetica 136: 27-36.
17. Devigili, A., Kelley, J.L., Pilastro, A. & Evans, J.P. 2013. Expression of pre- and postcopulatory traits under differential dietary conditions in guppies. Behav. Ecol. 24: 740-749.
18. Engqvist, L. 2008. Genetic variance and genotype reaction norms in response to larval food manipulation for a trait important in scorpionfly sperm competition. Funct. Ecol. 22: 127-133.
19. Evans, J.P. 2009. No evidence for sperm priming responses under varying sperm competition risk or intensity in guppies. Naturwissenschaften 96: 771-779.
20. Evans, J.P. 2010. Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc. R. Soc. Lond. B 277: 3195-3201.
21. Evans, J.P. 2011. Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies. Heredity 106: 869-875.
22. Evans, J.P. & Magurran, A.E. 2001. Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy. Proc. R. Soc. Lond. B 268: 719-724.
23. Evans, J.P. & Pilastro, A. 2011. Postcopulatory sexual selection. In: Ecology and Evolution of Poeciliid Fishes (J.P. Evans, A. Pilastro & I. Schlupp, eds), pp. 197-208. University of Chicago Press, Chicago, IL.
24. Evans, J.P., Zane, L., Francescato, S. & Pilastro, A. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421: 360-363.
25. Evans, J.P., Kelley, J.L., Bisazza, A., Finazzo, E. & Pilastro, A. 2004. Sire attractiveness influences offspring performance in guppies. Proc. R. Soc. Lond. B 271: 2035-2042.
26. Evans, J.P., van Lieshout, E. & Gasparini, C. 2013. Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia. Proc. R. Soc. Lond. B 280: 20130749.
27. Fitzpatrick, J.L. & Evans, J.P. 2014. Postcopulatory inbreeding avoidance in guppies. J. Evol. Biol. 27: 2585-2594.
28. Fry, J.D., Heinsohn, S.L. & Mackay, T.F.C. 1996. The contribution of new mutations to genotype-environment interaction for fitness in Drosophila melanogaster. Evolution 50: 2316-2327.
29. Garcia-Gonzalez, F., Simmons, L.W., Tomkins, J.L., Kotiaho, J.S. & Evans, J.P. 2012. Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66: 2341-2349.
30. Gardiner, D.M. 1978. Utilization of extracellular glucose by spermatozoa of two viviparous fishes. Comp. Biochem. Physiol. 59A: 165-168.
31. Gasparini, C., Peretti, A.V. & Pilastro, A. 2009. Female presence influences sperm velocity in the guppy. Biol. Lett. 5: 792-794.
32. Gasparini, C., Devigili, A., Dosselli, R. & Pilastro, A. 2013. Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits. Ecol. Evol. 3: 4940-4953.
33. Gibson, J.S. & Uetz, G.W. 2012. Effect of rearing environment and food availability on seismic signalling in male wolf spiders (Araneae: Lycosidae). Anim. Behav. 84: 85-92.
34. Gienapp, P. & Merila, J. 2010. Genetic and environmental effects on a condition-dependent trait: feather growth in Siberian jays. J. Evol. Biol. 23: 715-723.
35. Greenfield, M.D., Danka, R.G., Gleason, J.M., Harris, B.R. & Zhou, Y. 2012. Genotype x environment interaction, environmental heterogeneity and the lek paradox. J. Evol. Biol. 25: 601-613.
36. Grether, G. 2000. Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54: 1712-1724.
37. Hain, T.J.A. & Neff, B.D. 2007. Multiple paternity and kin recognition mechanisms in a guppy population. Mol. Ecol. 16: 3938-3946.
38. Higginson, A.D. & Reader, T. 2009. Environmental heterogeneity, genotype-by-environment interactions and the reliability of sexual traits as indicators of mate quality. Proc. R. Soc. B-Biol. Sci. 276: 1153-1159.
39. Holzer, B., Jacot, A. & Brinkhof, M.W.G. 2003. Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav. Ecol. 14: 353-359.
40. Houde, A.E. 1992. Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulata (Pisces: Poeciliidae) (guppies). Heredity 69: 229-235.
41. Houde, A.E. 1997. Sex, Color, and Mate Choice in Guppies. Princeton University Press, Princeton NJ.
42. Hughes, K.A., Rodd, F.H. & Reznick, D.N. 2005. Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). J. Evol. Biol. 18: 35-45.
43. Hunt, J. & Hosken, D.J., eds 2014. Genotype-by-Environment Interactions and Sexual Selection. Wiley Blackwell, Chichester.
44. Hunt, J., Bussière, L.F., Jennions, M.D. & Brooks, R. 2004. What is genetic quality? Trends Ecol. Trends Ecol. Evol. 19: 329-333.
45. Ingleby, F.C., Hunt, J. & Hosken, D.J. 2010. The role of genotype-by-environment interactions in sexual selection. J. Evol. Biol. 23: 2031-2045.
46. Ingleby, F.C., Hosken, D.J., Flowers, K., Hawkes, M.F., Lane, S.M., Rapkin, J. et al. 2013. Genotype-by-environment interactions for cuticular hydrocarbon expression in Drosophila simulans. J. Evol. Biol. 26: 94-107.
47. Ingleby, F.C., Hosken, D.J., Flowers, K., Hawkes, M.F., Lane, S.M., Rapkin, J. et al. 2014. Environmental heterogeneity, multivariate sexual selection and genetic constraints on cuticular hydrocarbons in Drosophila simulans. J. Evol. Biol. 27: 700-713.
48. Karino, K. & Haijima, Y. 2004. Algal-diet enhances sexual ornament, growth and reproduction in the guppy. Behaviour 141: 585-601.
49. Kemp, D.J. & Rutowski, R.L. 2007. Condition dependence, quantitative genetics, and the potential signal content of iridescent ultraviolet butterfly coloration. Evolution 61: 168-183.
50. Kodric-Brown, A. 1989. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol. 25: 393-401.
51. Kokko, H., Brooks, R., Jennions, M.D. & Morley, J. 2003. The evolution of mate choice and mating biases. Proc. R. Soc. Lond. B 270: 653-664.
52. Kolluru, G.R. 2014. Genotype-by-Environment interactions and sexual selection in guppies. In: Genotype-by-environment Interactions and Sexual Selection (J. Hunt & D.J. Hosken, eds), pp. 282-311. Wiley Blackwell, Chichester.
53. Kotiaho, J.S., Simmons, L.W. & Tomkins, J.L. 2001. Towards a resolution of the lek paradox. Nature 410: 684-686.
54. Kotiaho, J.S., Simmons, L.W., Hunt, J. & Tomkins, J.L. 2003. Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus. Am. Nat. 161: 852-859.
55. Kuckuck, C. & Greven, H. 1997. Notes on the mechanically stimulated discharge of spermiozeugmata in the guppy, Poecilia reticulata: a quantitative approach. Z. für Fisch. 4: 73-88.
56. Lande, R. & Arnold, S.J. 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226.
57. Lewandowski, E. & Boughman, J.W. 2008. Effects of genetics and light environment on colour expression in threespine sticklebacks. Biol. J. Linn. Soc. 94: 663-673.
58. Lewis, S.M., Tigreros, N., Fedina, T. & Ming, Q.L. 2012. Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles. J. Evol. Biol. 25: 438-451.
59. Locatello, L., Rasotto, M.B., Evans, J.P. & Pilastro, A. 2006. Colourful male guppies produce faster and more viable sperm. J. Evol. Biol. 19: 1595-1602.
60. Matthews, I.M., Evans, J.P. & Magurran, A.E. 1997. Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proc. R. Soc. Lond. B 264: 695-700.
61. 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.
62. Miller, L.K. & Brooks, R. 2005. The effects of genotype, age, and social environment on male ornamentation, mating behavior, and attractiveness. Evolution 59: 2414-2425.
63. Mills, S.C., Alatalo, R.V., Koskela, E., Mappes, J., Mappes, T. & Oksanen, T.A. 2007. Signal reliability compromised by genotype-by-environment interaction and potential mechanisms for its preservation. Evolution 61: 1748-1757.
64. Morrow, E.H., Leijon, A. & Meerupati, A. 2008. Hemiclonal analysis reveals significant genetic, environmental and genotype × environment effects on sperm size in Drosophila melanogaster. J. Evol. Biol. 21: 1692-1702.
65. Neff, B.D., Pitcher, T.E. & Ramnarine, I.W. 2008. Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol. Ecol. 17: 2975-2984.
66. Pilastro, A., Evans, J.P., Sartorelli, S. & Bisazza, A. 2002. Male phenotype predicts insemination success in guppies. Proc. R. Soc. Lond. B 269: 1325-1330.
67. Pitcher, T.E. & Evans, J.P. 2001. Male phenotype and sperm number in the guppy (Poecilia reticulata). Can. J. Zool. 79: 1891-1896.
68. Pitcher, T.E., Neff, B.D., Rodd, F.H. & Rowe, L. 2003. Multiple mating and sequential mate choice in guppies: females trade up. Proc. R. Soc. Lond. B 270: 1623-1629.
69. Pitcher, T.E., Rodd, F.H. & Rowe, L. 2007. Sexual colouration and sperm traits in guppies. J. Fish Biol. 70: 165-177.
70. Pomiankowski, A. & Møller, A.P. 1995. A resolution of the lek paradox. Proc. R. Soc. Lond. B 260: 21-29.
71. R Development Core Team 2014. A Language and Environment for Statistical Computing, Version 3.1.0. R Foundation for Statistical Computing, Vienna, Austria: URL http://www.R-project.org/.
72. Rahman, M., Kelley, J.L. & Evans, J.P. 2013. Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecol. Evol. 3: 2197-2213.
73. Rahman, M.M., Turchini, G.M., Gasparini, C., Norambuena, F. & Evans, J.P. 2014. The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies. PLoS ONE 9: e105856.
74. Robinson, M.R., Wilson, A.J., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. 2009. The impact of environmental heterogeneity on genetic architecture in a wild population of soay sheep. Genetics 181: 1639-1648.
75. Roff, D.A. 2002. Life History Evolution. Sinauer Associates Inc, Sunderland, MA.
76. Roff, D.A. 2008. Comparing sire and dam estimates of heritability: jackknife and likelihood approaches. Heredity 100: 32-38.
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. Sgro, C.M. & Hoffmann, A.A. 2004. Genetic correlations, tradeoffs and environmental variation. Heredity 93: 241-248.
79. Taylor, M.L., Evans, J.P. & Garcia-Gonzalez, F. 2013. No evidence for heritability of male mating latency or copulation duration across social environments in Drosophila melanogaster. PLoS ONE 8: e77347.
80. Tomkins, J.L., Radwan, J., Kotiaho, J.S. & Tregenza, T. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19: 323-328.
81. Wade, M.J. 2014. Genotype-by-environment interactions and sexual selection: female choice in a complex world. In: Genotype-by-Environment Interactions and Sexual Selection (J. Hunt & D.J. Hosken, eds), pp. 3-18. Wiley-Blackwell, Chichester.
82. Wilson-Leedy, J.G. & Ingermann, R.L. 2007. Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67: 661-672.