Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits

Ecology and Evolution

Volumn 3, Issue 15, 2013, Pages 4940-4953

  Gasparini, Clelia ^a,b   Devigili, Alessandro ^a   Dosselli, Ryan ^a,b   Pilastro, Andrea ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Genetic benefits; Good sperm models; Lek paradox; Polyandry; Sperm competition

Indexed keywords

EID: 84889681707     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.870     Document Type: Article

References (101)

1. Ala-Honkola, O., D. J. Hosken, M. K. Manier, S. Lüpold, E. M. Droge-Young, K. S. Berben, et al. 2013. Inbreeding reveals mode of past selection on male reproductive characters in Drosophila melanogaster. Ecol. Evol. 3:2089-2102.
2. Almbro, M., D. K. Dowling, and L. W. Simmons. 2011. Effects of vitamin E and beta-carotene on sperm competitiveness. Ecol. Lett. 14:891-895.
3. Andersson, M. 1986. Evolution of condition dependent sex ornaments and mating preferences: sexual selection based on viability differences. Biol. J. Linn. Soc. 40:804-816.
4. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
5. Barbosa, M., S. Connolly, M. Hisano, M. Dornelas, and A. Magurran. 2012. Fitness consequences of female multiple mating: a direct test of indirect benefits. BMC Evol. Ecol. 12:185.
6. Becker, W. A. 1984. A manual of quantitative genetics. Academic Enterprises, Pullman, WA.
7. Birkhead, T. R., and A. P. Møller. 1998. Sperm competition and sexual selection. Academic Press, London.
8. Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3:262-273.
9. Birkhead, T. R., E. J. Pellatt, P. Brekke, R. Yeates, and H. Castillo-Juarez. 2005. Genetic effects on sperm design in the zebra finch. Nature 434:383-387.
10. Birkhead, T. R., D. J. Hosken, and S. Pitnick. 2009. Sperm biology. Academic Press, London.
11. Boschetto, C., C. Gasparini, and A. Pilastro. 2011. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65:813-821.
12. Bozynski, C. C., and N. R. Liley. 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.
13. Brakefield, P. M., E. El Filali, R. Van Der Laan, C. J. Breuker, I. J. Saccheri, and B. Zwaan. 2001. Effective population size, reproductive success and sperm precedence in the butterfly, Bicyclus anynana, in captivity. J. Evol. Biol. 14:148-156.
14. Brooks, R., and J. A. Endler. 2001a. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002-1015.
15. Brooks, R., and J. A. Endler. 2001b. Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection. Evolution 55:1644-1655.
16. Candolin, U. 2003. The use of multiple cues in mate choice. Biol. Rev. 78:575-595.
17. Charlesworth, B., and D. Charlesworth. 1999. The genetic basis of inbreeding depression. Genet. Res. 74:329-340.
18. Clark, E. 1950. A method for artificial insemination in viviparous fishes. Science 112:722-723.
19. Cotton, S., K. Fowler, and A. Pomiankowski. 2004. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. B. Lond. 271:771-783.
20. Crnokrak, P., and D. A. Roff. 1995. Dominance variance: associations with selection and fitness. Heredity 75:530-540.
21. Darwin, C. 1859. The origin of species by means of natural selection. Murray, London.
22. Delcourt, M., and H. D. Rundle. 2011. Condition dependence of a multicomponent sexual display trait in Drosophila serrata. Am. Nat. 177:812-823.
23. Devigili, A., J. L. Kelley, A. Pilastro, and J. P. Evans. 2013. Expression of pre- and postcopulatory traits under different dietary conditions in guppies. Behav. Ecol. 24:740-749.
24. Evans, J. P. 2010. Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc. R. Soc. B. Lond. 277:3195-3201.
25. Evans, J. P. 2011. Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies. Heredity 106:869-875.
26. Evans, J. P., and A. E. Magurran. 2000. Multiple benefits of multiple mating in guppies. Proc. Natl Acad. Sci. USA 97:10074-10076.
27. Evans, J. P., and A. Pilastro. 2011. Postcopulatory sexual selection. Pp. 197-208 in J. P. Evans, A. Pilastro and I. Schlupp, eds. Ecology and evolution of poeciliid fishes. Chicago Univ. Press, Chicago.
28. Evans, J. P., L. Zane, S. Francescato, and A. Pilastro. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360-363.
29. Evans, J. P., J. L. Kelley, A. Bisazza, E. Finazzo, and A. Pilastro. 2004. Sire attractiveness influences offspring performance in guppies. Proc. R. Soc. B. Lond. 271:2035-2042.
30. Falconer, D. S., and T. F. C. Mackay 1996. Introduction to quantitative genetics, Longman, New York.
31. Fitzpatrick, J. L., and J. P. Evans. 2009. Reduced heterozygosity impairs sperm quality in endangered mammals. Biol. Lett. 5:320-323.
32. Gage, M. J. G., and P. A. Cook. 1994. Sperm size or numbers: effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera, Pyralidae). Funct. Ecol. 8:594-599.
33. Garcia, C. M., and E. Ramirez. 2005. Evidence that sensory traps can evolve into honest signals. Nature 434:501-505.
34. Garcia-Gonzalez, F., L. W. Simmons, J. L. Tomkins, J. S. Kotiaho, and J. P. Evans. 2012. Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66:2341-2349.
35. Gasparini, C., and A. Pilastro. 2011. Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. R. Soc. B. Lond. 278:2495-2501.
36. Gasparini, C., A. V. Peretti, and A. Pilastro. 2009. Female presence influences sperm velocity in the guppy. Biol. Lett. 5:792-794.
37. Gasparini, C., I. A. M. Marino, C. Boschetto, and A. Pilastro. 2010a. Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata). J. Evol. Biol. 23:124-135.
38. Gasparini, C., L. W. Simmons, M. Beveridge, and J. P. Evans. 2010b. Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS ONE 5:e12146.
39. Gilmour, A. R., B. J. Gogel, B. R. Cullis, and R. Thompson 2009. ASReml user guide release 3.0, VSN International Ltd, Hemel Hempstead
40. Grafen, A. 1990. Sexual selection unhandicapped by the Fisher process. J. Theor. Biol. 144:475-516.
41. Grorud-Colvert, K., and S. Sponaugle. 2006. Influence of condition on behavior and survival potential of a newly settled coral reef fish, the bluehead wrasse Thalassoma bifasciatum. Mar. Ecol. Prog. Ser. 327:279.
42. Hayward, A., and J. F. Gillooly. 2011. The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6:e16557.
43. Hine, E., S. Lachish, M. Higgie, and M. W. Blows. 2002. Positive genetic correlation between female preference and offspring fitness. Proc. R. Soc. B. Lond. 269:2215-2219.
44. Hoekstra, H. E., J. M. Hoekstra, D. Berrigan, S. N. Vignieri, A. Hoang, C. E. Hill, et al. 2001. Strength and tempo of directional selection in the wild. Proc. Natl Acad. Sci. USA 98:9157-9160.
45. Houde, A. E. 1997. Sex, color, and mate choice in guppies. Princeton Univ. Press, Princeton, NJ.
46. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
47. Houle, D. 1998. How should we explain variation in the genetic variance of traits? Genetica 103:241-253.
48. Immler, S., S. Pitnick, G. A. Parker, K. L. Durrant, S. Lüpold, S. Calhim, et al. 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc. Natl Acad. Sci. USA 108:5325-5330.
49. Iwasa, Y., A. Pomiankowski, and S. Nee. 1991. The evolution of costly mate preferences II. The 'handicap' principle. Evolution 45:1431-1442.
50. Johnson, T., and N. Barton. 2005. Theoretical models of selection and mutation on quantitative traits. Philos. Trans. R. Soc. B 360:1411-1425.
51. Kelly, J. K. 1999. An experimental method for evaluating the contribution of deleterious mutations to quantitative trait variation. Genet. Res. 73:263-273.
52. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, et al. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157:245-261.
53. Knell, R. J., and L. W. Simmons. 2010. Mating tactics determine patterns of condition dependence in a dimorphic horned beetle. Proc. R. Soc. B. Lond. 277:2347-2353.
54. Konior, M., L. Keller, and J. Radwan. 2005. Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini. Heredity 94:577-581.
55. Kotiaho, J. S., L. W. Simmons, J. Hunt, and J. L. Tomkins. 2003. Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus. Am. Nat. 161:852-859.
56. Kotiaho, J. S., N. R. Lebas, M. Puurtinen, and J. L. Tomkins. 2008. On the resolution of the lek paradox. Trends Ecol. Evol. 23:1-3.
57. Kunzler, R., and T. C. M. Bakker. 2001. Female preferences for single and combined traits in computer animated stickleback males. Behav. Ecol. 12:681-685.
58. Kvarnemo, C., and L. W. Simmons. 2013. Polyandry as a mediator of sexual selection before and after mating. Philos. Trans. R. Soc. B 368:20120042.
59. Lessells, C. M., and P. T. Boag. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104:116-121.
60. Lewis, Z., and N. Wedell. 2007. Effect of adult feeding on male mating behaviour in the butterfly, Bicyclus anynana (Lepidoptera: Nymphalidae). J. Insect Behav. 20:201-213.
61. Lewis, Z., H. Sasaki, and T. Miyatake. 2011. Sex starved: do resource-limited males ensure fertilization success at the expense of precopulatory mating success? Anim. Behav. 81:579-583.
62. Lindholm, A. K., F. Breden, H. J. Alexander, W. K. Chan, S. G. Thakurta, and R. Brooks. 2005. Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol. Ecol. 14:3671-3682.
63. Lüpold, S., M. K. Manier, K. S. Berben, K. J. Smith, B. D. Daley, S. H. Buckley, et al. 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr. Biol. 22:1667-1672.
64. Lynch, M., and J. B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
65. Magurran, A. E., and B. H. Seghers. 1994. Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc. R. Soc. B. Lond. 255:31-36.
66. Michalczyk, L., O. Y. Martin, A. L. Millard, B. C. Emerson, and M. J. G. Gage. 2010. Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proc. R. Soc. B. Lond. 277:3483-3491.
67. Miller, L. K., and R. Brooks. 2005. The effects of genotype, age, and social environment on male ornamentation, mating behavior, and attractiveness. Evolution 59:2414-2425.
68. Moore, P. J., W. E. Harris, V. T. Montrose, D. Levin, and A. J. Moore. 2004. Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58:1773-1780.
69. Neff, B. D., T. E. Pitcher, and I. W. Ramnarine. 2008. Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol. Ecol. 17:2975-2984.
70. Ojanguren, A. F., J. P. Evans, and A. E. Magurran. 2005. Multiple mating influences offspring size in guppies. J. Fish Biol. 67:1184-1188.
71. Olsson, M., T. Madson, and R. Shine. 1997. Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. B. Lond. 264:455-459.
72. Orr, T. J., and M. Zuk. 2012. Sperm storage. Curr. Biol. 22:R8-R10.
73. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525-567.
74. Pilastro, A., and A. Bisazza. 1999. Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc. R. Soc. B. Lond. 266:1887-1891.
75. Pilastro, A., C. Gasparini, C. Boschetto, and J. P. Evans. 2008. Colorful male guppies do not provide females with fecundity benefits. Behav. Ecol. 19:374-381.
76. Pitnick, S., T. A. Markow, and G. S. Spicer. 1995. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl Acad. Sci. USA 92:10614-10618.
77. Pomiankowski, A. 1987. Sexual selection: the handicap principal does work sometimes. Proc. R. Soc. B. Lond. 231:123-145.
78. Pomiankowski, A., and A. P. Møller. 1995. A resolution of the lek paradox. Proc. R. Soc. B. Lond. 260:21-29.
79. Radwan, J. 2008. Maintenance of genetic variation in sexual ornaments: a review of the mechanisms. Genetica 134:113-127.
80. Rahman, M. M., J. L. Kelley, and J. P. Evans. 2013. Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecol Evol 3:2197-2213.
81. Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. B. Lond. 263:1415-1421.
82. Shuster, S. M., and M. J. Wade. 2003. Mating systems and strategies. Princeton Univ. Press, Princeton, NJ.
83. Simmons, L. W. 2001. The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J. Evol. Biol. 14:585-594.
84. Simmons, L. W. 2005. The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu. Rev. Ecol. Evol. Syst. 36:125-146.
85. Simmons, L. W. 2011. Inbreeding depression in the competitive fertilization success of male crickets. J. Evol. Biol. 24:415-421.
86. Simmons, L. W., and D. J. Emlen. 2006. Evolutionary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103:16346-16351.
87. Simmons, L. W., and J. S. Kotiaho. 2002. Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622-1631.
88. Simmons, L. W., and J. S. Kotiaho. 2007. Quantitative genetic correlation between trait and preference supports a sexually selected sperm process. Proc. Natl Acad. Sci. USA 104:16604-16608.
89. Simmons, L. W., and A. J. Moore. 2009. Evolutionary quantitative genetics of sperm. Pp. 405-434 in R. B. Tim, J. H. David and P. Scott, eds. Sperm biology. Academic Press, London.
90. Simpson, J. L., S. Humphries, J. P. Evans, L. W. Simmons, and J. L. Fitzpatrick. 2013. Relationships between sperm length and speed differ among three internally and three externally fertilizing species. Evolution. Early view. doi:10.1111/evo.12199.
91. Smith, C. C. 2012. Opposing effects of sperm viability and velocity on the outcome of sperm competition. Behav. Ecol. 23:820-826.
92. Snook, R. R., L. D. Bacigalupe, and A. J. Moore. 2010. The quantitative genetics and coevolution of male and female reproductive traits. Evolution 64:1926-1934.
93. Thomsen, R., J. Soltis, M. Matsubara, K. Matsubayashi, M. Onuma, and O. Takenaka. 2006. How costly are ejaculates for Japanese macaques? Primates 47:272-274.
94. Thuler, K., L. F. Bussiere, E. Postma, P. I. Ward, and W. U. Blanckenhorn. 2011. Genetic and environmental sources of covariance among internal reproductive traits in the yellow dung fly. J. Evol. Biol. 24:1477-1486.
95. Tomkins, J. L., J. Radwan, J. S. Kotiaho, and T. Tregenza. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19:323-328.
96. Walsh, B., and M. W. Blows. 2009. Abundant genetic variation plus strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu. Rev. Ecol. Evol. Syst. 40:41-59.
97. Yasui, Y. 1997. A ''good-sperm'' model can explain the evolution of costly multiple mating by females. Am. Nat. 149:573-584.
98. Zahavi, A. 1975. Mate selection - a selection for a handicap. J. Theor. Biol. 53:205-214.
99. Zajitschek, S. R. K., and R. C. Brooks. 2008. Distinguishing the effects of familiarity, relatedness, and color pattern rarity on attractiveness and measuring their effects on sexual selection in guppies (Poecilia reticulata). Am. Nat. 172:843-854.
100. Zajitschek, S. R. K., and R. C. Brooks. 2010. Inbreeding depression in male traits and preference for outbred males in Poecilia reticulata. Behav. Ecol. 21:884-891.
101. Zajitschek, S. R. K., A. K. Lindholm, J. P. Evans, and R. C. Brooks. 2009. Experimental evidence that high levels of inbreeding depress sperm competitiveness. J. Evol. Biol. 22:1338-1345.