Covariation and repeatability of male mating effort and mating preferences in a promiscuous fish

Abstract

Although mate choice by males does occur in nature, our understanding of its importance in driving evolutionary change remains limited compared with that for female mate choice. Recent theoretical models have shown that the evolution of male mate choice is more likely when individual variation in male mating effort and mating preferences exist and positively covary within populations. However, relatively little is known about the nature of such variation and its maintenance within natural populations. Here, using the Trinidadian guppy (Poecilia reticulata) as a model study system, we report that mating effort and mating preferences in males, based on female body length (a strong correlate of fecundity), positively covary and are significantly variable among subjects. Individual males are thus consistent, but not unanimous, in their mate choice. Both individual mating effort (including courtship effort) and mating preference were significantly repeatable. These novel findings support the assumptions and predictions of recent evolutionary models of male mate choice, and are consistent with the presence of additive genetic variation for male mate choice based on female size in our study population and thus with the opportunity for selection and further evolution of large female body size through male mate choice.

References Abrahams, M. V. 1993. The trade-off between foraging and courting in male guppies. Anim. Behav. 45:673–681. Amundsen, T. 2000. Why are female birds ornamented?. Trends Ecol. Evol. 15:149–155. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ. Bakker, T. C. M., and A. Pomiankowski. 1995. The genetic basis of female mate preferences. J. Evol. Biol. 8:129–171. Bell, A. M., S. J. Hankinson, and K. L. Laskowski. 2009. The repeatability of behaviour: a meta-analysis. Anim. Behav. 77:771–783. Bel-Venner, M. C., S. Dray, D. Allaine, F. Menu, and S. Venner. 2008. Unexpected male choosiness for mates in a spider. Proc. R. Soc. Biol. Sci. 275:77–82. Boake, C. R. B. 1989. Repeatability: its role in evolutionary studies of mating behavior. Evol. Ecol. 3:173–182. Bonduriansky, R. 2001. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol. Rev. 76:305–339. Bretman, A., M. J. G. Gage, and T. Chapman. 2011. Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol. Evol. 26:467–473. Chenoweth, S. F., and M. W. Blows. 2006. Dissecting the complex genetic basis of mate choice. Nat. Rev. Genet. 7:681–692. Clutton-Brock, T. 2007. Sexual selection in males and females. Science 318:1882–1885. Clutton-Brock, T. H., and A. C. J. Vincent. 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60. Crawley, M. J. 2007. The R book. John Wiley and Sons Ltd., Chichester, U.K. Dohm, M. R. 2002. Repeatability measures do not always set an upper limit to heritability. Funct. Biol. 16:273–280. Dosen, L. D., and R. Montgomerie. 2004a. Female size influences mate preferences of male guppies. Ethology 110:245–255. Dosen, L. D., and R. Montgomerie. 2004b. Mate preferences by male guppies (Poecilia reticulata) in relation to the risk of sperm competition. Behav. Ecol. Sociobiol. 55:266–271. Edward, D. A., and T. Chapman. 2011. The evolution and significance of male mate choice. Trends Ecol. Evol. 26:647–654. Edward, D. A., and T. Chapman. 2012. Measuring the fitness benefits of male mate choice in Drosophila melanogaster. Evolution 66:2646–2653. Evans, J. P., A, Pilastro, and I. W. Ramnarine. 2003a. Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata) populations. Biol. J. Linn. Soc. 78:605–612. Evans, J. P., L. Zane, S. Francescato, and A. Pilastro. 2003b. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360–363. Field, A., J. Miles, and Z. Field. 2012. Discovering statistics using R. Sage Publications Ltd., London, U.K. Godin, J.-G. J. 1995. Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229. Godin, J.-G. J., and L. A. Dugatkin. 1995. Variability and repeatability of female mating preference in the guppy. Anim. Behav. 49:1427–1433. Griffiths, S. W., and A. E. Magurran. 1997. Familiarity in schooling fish: how long does it take to acquire? Anim. Behav. 53:945–949. Guevara-Fiore, P., A. Skinner, and P. J. Watt. 2009. Do male guppies distinguish virgin females from recently mated ones? Anim. Behav. 77:425–431. Guevara-Fiore, P., J. Stapley, and P. J. Watt. 2010a. Mating effort and female receptivity: how do male guppies decide when to invest in sex? Behav. Ecol. Sociobiol. 64:1665–1672. Guevara-Fiore, P., J. Stapley, J. Krause, I. W. Ramnarine, and P. J. Watt. 2010b. Male mate-searching strategies and female cues: how do male guppies find receptive females? Anim. Behav. 79:1191–1197. Head, M. L., B. B. M. Wong, and R. Brooks. 2010. Sexual display and mate choice in an energetically costly environment. PLoS ONE 5:e15279. Herdman, E. J. E., C. D. Kelly, and J.-G. J. Godin. 2004. Male mate choice in the guppy (Poecilia reticulata): do males prefer larger females as mates? Ethology 110:97–111. Houde, A. E. 1997. Sex, color and mate choice in guppies. Princeton University Press, Princeton, NJ. Hoysak, D. J., and J.-G. J. Godin. 2007. Repeatability of male mate choice in the mosquitofish, Gambusia holbrooki. Ethology 113:1007–1018. Hughes, K. A., L. Du, F. H. Rodd, and D. N. Reznick. 1999. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim. Behav. 58:907–916. Jennions, M. D., and M. Petrie. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Biol. Rev. 72:282–327. Jeswiet, S. B., and J.-G. J. Godin. 2011. Validation of a method for quantifying male mating preferences in the guppy (Poecilia reticulata). Ethology 117:422–429. Jeswiet, S. B., S. S. Y. Lee-Jenkins, I. W. Ramnarine, and J.-G. J. Godin. 2011. Sperm competition risk and mate choice in male Trinidadian guppies, Poecilia reticulata. Anim. Behav. 81:639–644. Jeswiet, S. B., S. S. Y. Lee-Jenkins, and J.-G. J. Godin. 2012. Concurrent effects of sperm competition and female quality on male mate choice in the Trinidadian guppy (Poecilia reticulata). Behav. Ecol. 23:195–200. Kelley, J. L., J. A. Graves, and A. E. Magurran. 1999. Familiarity breeds contempt in guppies. Nature 401:661–662. Kelly, C. D., J.-G. J. Godin, and J. M. Wright. 1999. Geographical variation in multiple paternity within natural populations of the guppy (Poecilia reticulata). Proc. R. Soc. Biol. Sci. 266:2403–2408. Kodric-Brown, A., and P. F. Nicoletto. 2001. Female choice in the guppy (Poecilia reticulata): the interaction between male color and display. Behav. Ecol. Sociobiol. 50:346–351. Kolluru, G. R., G. F. Grether, E. Dunlop, and S. H. South. 2009. Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behav. Ecol. 20:131–137. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Inc., Sunderland, MA. Magurran, A. E. 2005. Evolutionary ecology: the Trinidadian guppy. Oxford University Press, Oxford, U.K. Mariette, M., J. L. Kelley, R. Brooks, and J. P. Evans. 2006. The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112:807–814. Matthews, I. M., J. P. Evans, and A. E. Magurran. 1997. Male display rate reveals ejaculate characteristics in the Trinidadian guppy (Poecilia reticulata). Proc. R. Soc. Biol. Sci. 264:695–700. Nakagawa, S., and H. Schielzeth. 2010. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85:935–956. 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. Nicoletto, P. F. 1993. Female sexual response to condition-dependent ornaments in the guppy, Poecilia reticulata. Anim. Behav. 46:441–450. Nicoletto, P. F. 1995. Offspring quality and female choice in the guppy, Poecilia reticulata. Anim. Behav. 49:377–387. Ojanguren, A. F., and A. E. Magurran. 2004. Uncoupling the links between male mating tactics and female attractiveness. Proc. R. Soc. Biol. Sci. (Suppl. 6)271:S427–S429. Ojanguren, A. F., J. P. Evans, and A. E. Magurran. 2005. Multiple mating influences offspring size in guppies. J. Fish Biol. 67:1184–1188. Parker, G. A. 1983. Mate quality and mating decisions. Pp. 141–166 in P. Bateson, ed. Mate choice. Cambridge University Press, Cambridge, U.K. Pilastro, A., and A. Bisazza. 1999. Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata. Proc. R. Soc. Biol. Sci. 266:1887–1891. Pilastro, A., J. P. Evans, S. Sartorelli, and A. Bisazza. 2002. Male phenotype predicts insemination success in guppies. Proc. R. Soc. Biol. Sci. 269:1325–1330. Qvarnström, A. 2001. Context-dependent genetic benefits from mate choice. Trends Ecol. Evol. 16:5–7. R Development Core Team. 2012. R: a language and environment for statistical computing, version 2.15.1. R Foundation for Statistical Computing, Vienna, Austria. Available at http://cran.r-project.org/ (accessed June 22, 2012). Reznick, D., and J. A. Endler. 1982. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36:160–177. Rowell, J. T., and M. R. Servedio. 2009. Gentlemen prefer blondes: the evolution of mate preference among strategically allocated males. Am. Nat. 173:12–25. Servedio, M. R., and R. Lande. 2006. Population genetic models of male and mutual mate choice. Evolution 60:674–685. South, S. H., G. Arnqvist, and M. R. Servedio. 2012. Female preference for male courtship effort can drive the evolution of male mate choice. Evolution 66:3722–3735. Walling, C. A., N. J. Royle, J. Lindström, and N. B. Metcalfe. 2010. Do female association preferences predict the likelihood of reproduction? Behav. Ecol. Sociobiol. 64:541–548. Wedell, N., M. J. G. Gage, and G. A. Parker. 2002. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17:313–320. Widemo, F., and S. A. Sæther. 1999. Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends Ecol. Evol. 14:26–31.