Treat ’em Mean, Keep ’em (sometimes) Keen: Evolution of Female Preferences for Dominant and Coercive Males Research Article Received: 10 May 2004 Accepted: 06 October 2004 DOI:
Cite this article as: Kokko, H. Evol Ecol (2005) 19: 123. doi:10.1007/s10682-004-7919-1 Abstract
How should females choose their mates if choice is not completely free, but at least partly dictated by outcomes of male–male competition, or sexual coercion? This question is of central importance when evaluating the relationship between sexually antagonistic ‘chase-away’ scenarios and models of more traditional female choice. Currently, there is a mismatch between theories: indirect benefits are seen to play a role in conventional mate choice, whereas they are not predicted to have an influence on the outcome if matings impose direct costs on females. This is at odds with the idea that resistance and preference are two sides of the same coin: either leads to a subset of males enjoying enhanced mating success. In the same way as choosy females benefit from mating with sexy males if this yields sexy sons, females could benefit from being manipulated or ‘seduced’, if the manipulative or seductive ability of males is heritable. Here I build a model where male dominance (or coerciveness) improves his mating success, and this relationship can be modified by female behaviour. This clarifies the definitions of resistance and preference: resisting females diminish the benefit a male gains from being dominant, while preferences enhance this pre-existing benefit enjoyed by dominant males. In keeping with earlier theory, females may evolve to resist costly mating attempts as a counterstrategy to male traits, particularly if male dominance is environmentally rather than genetically determined. Contrary to earlier results, however, indirect benefits are also predicted to influence female mating behaviour, and if sufficiently strong, they may produce female preferences for males that harm them.
Keywords dominance indirect benefits mathematical model quantitative genetics sexual coercion sexual conflict References Arnqvist, G., Rowe, L. 2002 Antagonistic co-evolution between the sexes in a group of insects Nature 415 787 789 Google Scholar Berglund, A., Rosenqvist, G. 2003 Sex role reversal in pipefish Adv. Study Behav 32 131 167 CrossRef Google Scholar Berglund, A, Bisazza, A., Pilastro, A. 1996 Armaments and ornaments: an evolutionary explanation of traits of dual utility Biol. J. Linn. Soc 58 385 399 CrossRef Google Scholar Bernasconi, G., Keller, L. 2001 Female polyandry affects their sons’ reproductive success in the red flour beetle Tribolium castaneum J. Evol. Biol 14 186 193 CrossRef Google Scholar Bisazza, A, Vaccari, G., Pilastro, A. 2001 Female mate choice in a mating system dominated by male sexual coercion Behav. Ecol 12 59 64 Google Scholar Cameron, E, Day, T., Rowe, L. 2003 Sexual conflict and indirect benefits J. Evol. Biol 16 1055 1060 CrossRef PubMed Google Scholar Candolin, U. 1999 Male-male competition facilitates female choice in sticklebacks Proc. Roy. Soc. Lond. B 266 785 789 CrossRef Google Scholar Chapman, T, Arnqvist, G, Bangham, J., Rowe, L. 2003 Sexual conflict Trends Ecol. Evol 18 41 47 CrossRef Google Scholar Chapman, T, Liddle, L.F., Kalb, J.M., Wolfner, M.F., Partridge, L. 1995 Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products Nature 373 241 244 CrossRef PubMed Google Scholar Clutton-Brock, T.H., Parker, G.A. 1995 Sexual coercion in animal societies Anim. Behav 49 1345 1365 CrossRef Google Scholar Cordero, C., Eberhard, W.G. 2003 Female choice of sexually antagonistic male adaptations: a critical review of some current research J. Evol. Biol 16 1 6 CrossRef PubMed Google Scholar Cox, C.R., Le Boeuf, B.J. 1977 Female incitation of male competition: a mechanism in sexual selection Am. Nat 111 317 335 CrossRef Google Scholar Crudgington, H.S., Siva-Jothy, M.T. 2000 Genital damage, kicking and early death: the battle of the sexes takes a sinister turn in the bean weevil Nature 407 855 856 CrossRef PubMed Google Scholar Cunningham, E.J.A., Birkhead, T.R. 1998 Sex roles and sexual selection Anim. Behav 56 1311 1321 CrossRef PubMed Google Scholar Double, M.C., Cockburn, A. 2003 Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males Proc. Roy. Soc. Lond. B 270 379 384 CrossRef Google Scholar Eberhard, W.G., Cordero, C. 2003 Sexual conflict and female choice Trends Ecol. Evol 18 438 439 CrossRef Google Scholar Forsgren, E. 1997 Female sand gobies prefer good fathers over dominant males Proc. Roy. Soc. Lond. B 264 1283 1286 CrossRef Google Scholar Friberg, U., Arnqvist, G. 2003 Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females J. Evol. Biol 16 797 811 CrossRef PubMed Google Scholar Gavrilets, S, Arnquist, G., Friberg, U. 2001 The evolution of female mate choice by sexual conflict Proc. Roy. Soc. Lond. B 268 531 539 CrossRef Google Scholar Getty, T. 1999 Chase-away sexual selection as noisy reliable signalling Evolution 53 299 302 Google Scholar Haley, M.P. 1994 Resource-holding power asymmetries, the prior residence effect, and reproductive payoffs in male northern elephant seal fights Behav. Ecol. Sociobiol 34 427 434 Google Scholar Hall, D.W., Kirkpatrick, M., West, B. 2000 Runaway sexual selection when female preferences are directly selected Evolution 54 1862 1869 PubMed Google Scholar Holland, B., Rice, W.R. 1998 Chase-away selection: antagonistic seduction vs. resistance Evolution 52 1 7 Google Scholar Houle, D., Kondrashov, A.S. 2002 Co-evolution of costly mate choice and condition-dependent display of good genes Proc. Roy. Soc. Lond. B 269 97 104 CrossRef Google Scholar Iwasa, Y, Pomiankowski, A., Nee, S. 1991 The evolution of costly mate preferences. II. The “handicap” principle Evolution 45 1431 1442 Google Scholar Jennions, M.D., Petrie, M. 2000 Why do females mate multiply?. A review of the genetic benefits Biol. Rev 75 21 64 CrossRef PubMed Google Scholar Jennions, M.D., Møller, A.P., Petrie, M. 2001 Sexually selected traits and adult survival: a meta-analysis Q. Rev. Biol 76 3 36 CrossRef PubMed Google Scholar Johnstone, R.A., Keller, L. 2000 How males gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating Am. Nat 156 368 377 CrossRef Google Scholar Jormalainen, V. 1998 Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict Q. Rev. Biol 73 275 304 CrossRef Google Scholar Kokko, H, Brooks, R, Jennions, M., Morley, J. 2003 The evolution of mate choice and mating biases Proc. Roy. Soc. Lond. B 270 653 664 CrossRef Google Scholar Kokko, H, Brooks, R, McNamara, J.M., Houston, A.I. 2002 The sexual selection continuum Proc. Roy. Soc. Lond. B 269 1331 1340 CrossRef Google Scholar Kokko, H., Monaghan, P. 2001 Predicting the direction of sexual selection Ecol. Lett 4 159 165 CrossRef Google Scholar Lande, R. 1981 Models of speciation by sexual selection on polygenic characters Proc. Natl. Acad. Sci. USA 78 3721 3725 Google Scholar Lee, P.L.M., Hays, G.C. 2004 Polyandry in a marine turtle: females make the best of a bad job Proc. Natl. Acad. Sci. USA 101 6530 6535 CrossRef PubMed Google Scholar Markow, T.A. 2000 Forced matings in natural populations of Drosophila Am. Nat 156 100 103 CrossRef PubMed Google Scholar Martin, O.Y., Hosken, D.J., Ward, P.I. 2004 Post-copulatory sexual selection and female fitness in Scathophaga stercoraria Proc. Roy. Soc. Lond. B 271 353 359 CrossRef Google Scholar McKinney, F., Evarts, S. 1998 Sexual coercion in waterfowl and other birds Parker, P.G. Burley, N.T. eds. Avian Reproductive Tactics: Female and Male Perspectives. Allen Lawrence 163 195 Google Scholar Moore, A.J., Moore, P.J. 1999 Balancing sexual selection through opposing mate choice and male competition Proc. Roy. Soc. Lond. B 266 711 716 CrossRef Google Scholar Moore, A.J., Gowaty, P.A., Wallin, W.G., Moore, P.J. 2001 Sexual conflict and the evolution of female mate choice and male social dominance Proc. Roy. Soc. Lond. B 268 517 523 CrossRef Google Scholar Morrow, E.H., Arnqvist, G., Pitnick, S. 2003 Adaptation versus pleiotropy: why do males harm their mates? Behav. Ecol 14 802 806 CrossRef Google Scholar Møller, A.P., Alatalo, R.V. 1999 Good-genes effects in sexual selection Proc. Roy. Soc. Lond. B 266 85 91 CrossRef Google Scholar Ophir, A.G., Galef, B.G., Jr. 2003 Female Japanese quail that ‘eavesdrop’ on fighting males prefer losers to winners Anim. Behav 66 399 407 CrossRef Google Scholar Pai, A., Yan, G. 2002 Polyandry produces sexy sons at the cost of daughters in red flour beetles Proc. Roy. Soc. Lond. B 269 361 368 CrossRef Google Scholar Parker, G.A. 1979 Sexual selection and sexual conflict Blum, M.S. Blum, N.A. eds. Sexual Selection and Reproductive Competition in Insects. Academic Press New York 123 166 Google Scholar Partridge, L., Hurst, L.D. 1998 Sex and conflict Science 281 2003 2008 CrossRef PubMed Google Scholar Payne, R.J.H., Pagel, M. 2001 Inferring the origins of state-dependent courtship traits Am. Nat 157 42 50 CrossRef Google Scholar Pizzari, T. 2003 Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird Behav. Ecol 47 593 601 CrossRef Google Scholar Pizzari, T., Birkhead, T.R. 2000 Female feral fowl eject sperm of subdominant males Nature 405 787 789 CrossRef PubMed Google Scholar Pizzari, T., Snook, R.R. 2003 Sexual conflict and sexual selection: chasing away paradigm shifts Evolution 57 1223 1236 PubMed Google Scholar Pomiankowski, A, Iwasa, Y., Nee, S. 1991 The evolution of costly mate preferences. I. Fisher and biased mutation Evolution 45 1422 1430 Google Scholar Qvarnström, A., Forsgren, E. 1998 Should females prefer dominant males? Trends Ecol. Evol 13 498 501 CrossRef Google Scholar Reinhardt, K, Naylor, R., Siva-Jothy, M.T. 2003 Reducing a cost of traumatic insemination: female bedbugs evolve a unique organ Proc. Roy. Soc. Lond. B 270 2371 2375 CrossRef Google Scholar Rowe, L. 1992 Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration Anim. Behav 44 189 202 CrossRef Google Scholar Stutt, A.D., Siva-Jothy, M.T. 2001 Traumatic insemination and sexual conflict in the bed bug Cimex lectularius Proc. Natl. Acad. Sci. USA 98 5683 5687 CrossRef PubMed Google Scholar Thornhill, R., Alcock, J. 1983The Evolution of Insect Mating Systems Harvard University Press Cambridge, MA Google Scholar Watson, P.J., Armqvist, G., Stallmann, R.R. 1998 Sexual conflict and the energetic costs of mating and mate choice in water striders Am. Nat 151 46 58 CrossRef Google Scholar Wedell, N., Tregenza, T. 1999 Successful fathers sire successful sons Evolution 53 620 625 Google Scholar Wong, B.B.M. 2004 Superior fighters make mediocre fathers in the Pacific blue-eye fish Anim. Behav 67 583 590 CrossRef Google Scholar
Wong B.B.M., Candolin, U. (in press) How is female choice affected by male competition? Biol. Rev.