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Evolutionary Biology

, Volume 40, Issue 4, pp 589–600 | Cite as

Estimating the Dynamics of Sexual Selection in Changing Environments

Research Article

Abstract

Measuring sexual selection in changing environments is challenging, as the targets and mechanisms of selection can vary with the environment. Here, we present the results of an unusually comprehensive study of the influence of human-disturbed habitat structure on sexual selection in the threespine stickleback Gasterosteus aculeatus. We included all episodes of sexual selection, used molecular parentage assignments, and applied several metrics of sexual selection. The results show that the influence of altered habitat structure on sexual selection dynamics is more complex than previously thought, with the influence varying among selection episodes and male groups. Increased habitat structure relaxed the opportunity for sexual selection across episodes, but incorrect conclusions were reached if the analysis was restricted to resource-holding males or based on mating success. A novel finding, revealed by the parentage analysis, is a reduction in sneak fertilization in disturbed environments. This relaxed the opportunity for sexual selection as sneaking had increased the skew in mating success in less structured habitats, because of nesting males with a high mating success sneaking the most. Thus, the influence of environmental change on an alternative reproductive behavior amplified alterations in sexual selection. This emphasizes the need to consider more hidden processes than previously done when investigating how human disturbances modify sexual selection.

Keywords

Habitat change Male–male competition Mate choice Multiple cues Selection indices Alternative reproductive behavior 

Notes

Acknowledgments

We thank Tiina Salesto and Miia Mannerla for assistance, Steven Shuster for advice on the calculation of opportunity for sexual selection metrics, Hannu Mäkinen for advice on the microsatellite primers, and Tvärminne Zoological Station for providing working facilities. The experimental procedures were approved by the Animal Care Committee of the University of Helsinki (86-06) and by the National Animal Experiment Board in Finland (STH421A). The work was funded by the Academy of Finland and the University of Helsinki to UC.

Supplementary material

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Supplementary material 1 (DOCX 21 kb)
11692_2013_9234_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 17 kb)

References

  1. Ahnesjö, I., Kvarnemo, C., & Merilaita, S. (2001). Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behavioral Ecology, 12(4), 397–401.CrossRefGoogle Scholar
  2. Arnold, S. J., & Duvall, D. (1994). Animal mating systems—a synthesis based on selection theory. American Naturalist, 143(2), 317–348.CrossRefGoogle Scholar
  3. Arnold, S. J., & Wade, M. J. (1984a). On the measurement of natural and sexual selection: Applications. Evolution, 38, 720–734.CrossRefGoogle Scholar
  4. Arnold, S. J., & Wade, M. J. (1984b). On the measurements of natural and sexual selection: Theory. Evolution, 38, 709–719.CrossRefGoogle Scholar
  5. Balenger, S. L., Johnson, L. S., & Masters, B. S. (2009). Sexual selection in a socially monogamous bird: Male color predicts paternity success in the mountain bluebird, Sialia currucoides. Behavioral Ecology and Sociobiology, 63(3), 403–411.CrossRefGoogle Scholar
  6. Bateman, A. J. (1948). Intra-sexual selection in Drosophila Heredity, 2, 349–368.Google Scholar
  7. Birkhead, T. R., & Møller, A. P. (1998). Sperm competition and sexual selection. London: Academic Press.Google Scholar
  8. Bitton, P. P., O’Brien, E. L., & Dawson, R. D. (2007). Plumage brightness and age predict extrapair fertilization success of male tree swallows, tachycineta bicolor. Animal Behaviour, 74, 1777–1784.CrossRefGoogle Scholar
  9. Bonduriansky, R., & Rowe, L. (2003). Interactions among mechanisms of sexual selection on male body size and head shape in a sexually dimorphic fly. Evolution, 57(9), 2046–2053.PubMedGoogle Scholar
  10. Boughman, J. W., Rundle, H. D., & Schluter, D. (2005). Parallel evolution of sexual isolation in sticklebacks. Evolution, 59(2), 361–373.PubMedGoogle Scholar
  11. Candolin, U. (2000). Increased signalling effort when survival prospects decrease: Male–male competition ensures honesty. Animal Behaviour, 60, 417–422.PubMedCrossRefGoogle Scholar
  12. Candolin, U. (2004a). Effects of algae cover on egg acquisition in male three-spined stickleback. Behaviour, 141, 1389–1399.CrossRefGoogle Scholar
  13. Candolin, U. (2004b). Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman. Evolution, 58(8), 1861–1864.PubMedGoogle Scholar
  14. Candolin, U. (2009). Population responses to anthropogenic disturbance: Lessons from three-spined stickleback Gasterosteus aculeatus in eutrophic habitats. Journal of Fish Biology, 75(8), 2108–2121.PubMedCrossRefGoogle Scholar
  15. Candolin, U., Engström-Öst, J., & Salesto, T. (2008). Human-induced eutrophication enhances reproductive success through effects on parenting ability in sticklebacks. Oikos, 117(3), 459–465.CrossRefGoogle Scholar
  16. Candolin, U., & Heuschele, J. (2008). Is sexual selection beneficial during adaptation to environmental change? Trends in Ecology & Evolution, 23(8), 446–452.CrossRefGoogle Scholar
  17. Candolin, U., Salesto, T., & Evers, M. (2007). Changed environmental conditions weaken sexual selection in sticklebacks. Journal of Evolutionary Biology, 20, 233–239.PubMedCrossRefGoogle Scholar
  18. Candolin, U., & Voigt, H. R. (2003). Size-dependent selection on arrival times in sticklebacks: Why small males arrive first. Evolution, 57, 862–871.PubMedGoogle Scholar
  19. Cockburn, A., Osmond, H. L., & Double, M. C. (2008). Swingin’ in the rain: Condition dependence and sexual selection in a capricious world. Proceedings of the Royal Society B-Biological Sciences, 275(1635), 605–612.CrossRefGoogle Scholar
  20. Cothran, R. D., Stiff, A. R., Jeyasingh, P. D., & Relyea, R. A. (2012). Eutrophication and predation risk interact to affect sexual trait expression and mating success. Evolution, 66(3), 708–719.PubMedCrossRefGoogle Scholar
  21. Croshaw, D. A. (2010). Quantifying sexual selection: A comparison of competing indices with mating system data from a terrestrially breeding salamander. Biological Journal of the Linnean Society, 99(1), 73–83.CrossRefGoogle Scholar
  22. Downhower, J. F., Blumer, L. S., & Brown, L. (1987). Opportunity for selection—an appropriate measure for evaluating variation in the potential for selection. Evolution, 41(6), 1395–1400.CrossRefGoogle Scholar
  23. Duval, E. H., & Kempenaers, B. (2008). Sexual selection in a lekking bird: The relative opportunity for selection by female choice and male competition. Proceedings of the Royal Society B-Biological Sciences, 275(1646), 1995–2003.CrossRefGoogle Scholar
  24. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection and the evolution of mating systems. Science, 197, 215–223.PubMedCrossRefGoogle Scholar
  25. Engström-Öst, J., & Candolin, U. (2007). Human-induced water turbidity alters selection on sexual displays in sticklebacks. Behavioral Ecology, 18, 393–398.CrossRefGoogle Scholar
  26. Fairbairn, D. J., & Wilby, A. E. (2001). Inequality of opportunity: Measuring the potential for sexual selection. Evolutionary Ecology Research, 3(6), 667–686.Google Scholar
  27. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. Essex: Longman.Google Scholar
  28. Fitze, P. S., & Le Galliard, J. F. (2011). Inconsistency between different measures of sexual selection. American Naturalist, 178(2), 256–268.PubMedCrossRefGoogle Scholar
  29. Garant, D., Sheldon, B. C., & Gustafsson, L. (2004). Climatic and temporal effects on the expression of secondary sexual characters: Genetic and environmental components. Evolution, 58(3), 634–644.PubMedGoogle Scholar
  30. Griffith, S. C., Owens, I. P. F., & Thuman, K. A. (2002). Extra pair paternity in birds: A review of interspecific variation and adaptive function. Molecular Ecology, 11(11), 2195–2212.PubMedCrossRefGoogle Scholar
  31. Hereford, J., Hansen, T. F., & Houle, D. (2004). Comparing strengths of directional selection: How strong is strong? Evolution, 58(10), 2133–2143.PubMedGoogle Scholar
  32. Heuschele, J., & Candolin, U. (2010). Reversed parasite-mediated selection in sticklebacks from eutrophied habitats. Behavioral Ecology and Sociobiology, 64(8), 1229–1237.CrossRefGoogle Scholar
  33. Heuschele, J., Mannerla, M., Gienapp, P., & Candolin, U. (2009). Environment-dependent use of mate choice cues in sticklebacks. Behavioral Ecology, 20(6), 1223–1227.CrossRefGoogle Scholar
  34. Heuschele, J., Salminen, T., & Candolin, U. (2012). Habitat change influences mate search behaviour in three-spined sticklebacks. Animal Behaviour, 83(2012), 1505–1510.CrossRefGoogle Scholar
  35. Holland, B., & Rice, W. R. (1999). Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proceedings of the National Academy of Sciences of the United States of America, 96(9), 5083–5088.PubMedCrossRefGoogle Scholar
  36. Hrdy, S. B. (1979). Infanticide among animals—review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology, 1(1), 13–40.CrossRefGoogle Scholar
  37. Hunt, J., Breuker, C. J., Sadowski, J. A., & Moore, A. J. (2009). Male-male competition, female mate choice and their interaction: Determining total sexual selection. Journal of Evolutionary Biology, 22(1), 13–26.PubMedGoogle Scholar
  38. Janzen, F. J., & Stern, H. S. (1998). Logistic regression for empirical studies of multivariate selection. Evolution, 52(6), 1564–1571.CrossRefGoogle Scholar
  39. Jennions, M. D., Kokko, H., & Klug, H. (2012). The opportunity to be misled in studies of sexual selection. Journal of Evolutionary Biology, 25, 591–598.PubMedCrossRefGoogle Scholar
  40. Jones, A. G. (2009). On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution, 63(7), 1673–1684.PubMedCrossRefGoogle Scholar
  41. Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5), 1099–1106.PubMedCrossRefGoogle Scholar
  42. Klug, H., Heuschele, J., Jennions, M. D., & Kokko, H. (2010a). The mismeasurement of sexual selection. Journal of Evolutionary Biology, 23(3), 447–462.PubMedGoogle Scholar
  43. Klug, H., Lindström, K., & Kokko, H. (2010b). Who to include in measures of sexual selection is no trivial matter. Ecology Letters, 13(9), 1094–1102.PubMedCrossRefGoogle Scholar
  44. Kokko, H., Klug, H., & Jennions, M. D. (2012). Unifying cornerstones of sexual selection: Operational sex ratio, Bateman gradient, and the scope for competitive investment. Ecology Letters, 15, 1340–1351.PubMedCrossRefGoogle Scholar
  45. Krakauer, A. H., Webster, M. S., Duval, E. H., Jones, A. G., & Shuster, S. M. (2011). The opportunity for sexual selection: Not mismeasured, just misunderstood. Journal of Evolutionary Biology, 24(9), 2064–2071.PubMedGoogle Scholar
  46. Kvarnemo, C., & Ahnesjö, I. (1996). The dynamics of operational sex ratios and competition for mates. Trends in Ecology & Evolution, 11(10), 404–408.CrossRefGoogle Scholar
  47. Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37, 1210–1226.CrossRefGoogle Scholar
  48. Largiader, C. R., Fries, V., & Bakker, T. C. M. (2001). Genetic analysis of sneaking and egg-thievery in a natural population of the three-spined stickleback (Gasterosteus aculeatus L.). Heredity, 86, 459–468.PubMedCrossRefGoogle Scholar
  49. Lengagne, T. (2008). Traffic noise affects communication behaviour in a breeding anuran, Hyla arborea. Biological Conservation, 141(8), 2023–2031.CrossRefGoogle Scholar
  50. Long, T. A. F., Agrawal, A. F., & Rowe, L. (2012). The effect of sexual selection on offspring fitness depends on the nature of genetic variation. Current Biology, 22(3), 204–208.PubMedCrossRefGoogle Scholar
  51. Mehlis, M., Bakker, T. C. M., Engqvist, L., & Frommen, J. G. (2010). To eat or not to eat: Egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism. Proceedings of the Royal Society B-Biological Sciences, 277(1694), 2627–2635.CrossRefGoogle Scholar
  52. Møller, A. P. (2004). Protandry, sexual selection and climate change. Global Change Biology, 10(12), 2028–2035.CrossRefGoogle Scholar
  53. Moore, A. J., & Moore, P. J. (1999). Balancing sexual selection through opposing mate choice and male competition. Proceedings of the Royal Society of London Series B-Biological Sciences, 266(1420), 711–716.CrossRefGoogle Scholar
  54. Oliveira, R., Taborsky, M., & Brockmann, H. J. (2008). Alternative reproductive tactics: An integrative approach. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  55. Reichard, M., Ondrackova, M., Bryjova, A., Smith, C., & Bryja, J. (2009). Breeding resource distribution affects selection gradients on male phenotypic traits: Experimental study on lifetime reproductive success in the bitterling fish (Rhodeus amarus). Evolution, 63(2), 377–390.PubMedCrossRefGoogle Scholar
  56. Rowland, W. J. (1989). The effects of body size, aggression and nuptial coloration on competition for territories in male threespine sticklebacks, Gasterosteus aculeatus. Animal Behaviour, 132, 282–289.CrossRefGoogle Scholar
  57. Rundus, A. S., Sullivan-Beckers, L., Wilgers, D. J., & Hebets, E. A. (2011). Females are choosier in the dark: environment-dependent reliance on courtship components and its impact on fitness. Evolution, 65(1), 268–282.PubMedCrossRefGoogle Scholar
  58. Schradin, C., & Lindholm, A. K. (2011). Relative fitness of alternative male reproductive tactics in a mammal varies between years. Journal of Animal Ecology, 80(5), 908–917.PubMedCrossRefGoogle Scholar
  59. Seehausen, O., Alphen, J. J. M., & Witte, F. (1997). Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808–1811.CrossRefGoogle Scholar
  60. Sefc, K. M., Mattersdorfer, K., Sturmbauer, C., & Koblmuller, S. (2008). High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence. Molecular Ecology, 17(10), 2531–2543.PubMedCrossRefGoogle Scholar
  61. Shuker, D. M. (2010). Sexual selection: Endless forms or tangled bank? Animal Behaviour, 79(3), E11–E17.CrossRefGoogle Scholar
  62. Shuster, S. M. (2009). Sexual selection and mating systems. Proceedings of the National Academy of Sciences of the United States of America, 106, 10009–10016.PubMedCrossRefGoogle Scholar
  63. Shuster, S. M., & Wade, M. J. (2003). Mating systems and strategies. Princeton, NJ.: Princeton University Press.Google Scholar
  64. Soulsbury, C. D. (2010). Genetic patterns of paternity and testes size in mammals. PLoS ONE, 5(3), A152–A157.CrossRefGoogle Scholar
  65. Sundin, J., Berglund, A., & Rosenqvist, G. (2010). Turbidity hampers mate choice in a pipefish. Ethology, 116(8), 713–721.Google Scholar
  66. Sutherland, W. J. (1985). Chance can produce a sex difference in variance in mating success and explain Batemans data. Animal Behaviour, 33, 1349–1352.CrossRefGoogle Scholar
  67. Taborsky, M. (1998). Sperm competition in fish: ‘Bourgeois’ males and parasitic spawning. Trends in Ecology & Evolution, 13, 222–227.CrossRefGoogle Scholar
  68. Uller, T., & Olsson, M. (2008). Multiple paternity in reptiles: Patterns and processes. Molecular Ecology, 17(11), 2566–2580.PubMedCrossRefGoogle Scholar
  69. van den Assem, J. (1967). Territoriality in the threespine stickleback, Gasterosteus aculeatus L.: An experimental study in intra-specific competition. Behaviour, 16, 1–164.Google Scholar
  70. Vlieger, L., & Candolin, U. (2009). How not to be seen: Does eutrophication influence stickleback sneaking behaviour? Journal of Fish Biology, 75, 2163–2174.PubMedCrossRefGoogle Scholar
  71. Wade, M. J. (1979). Sexual selection and variance in reproductive success. American Naturalist, 114(5), 742–747.CrossRefGoogle Scholar
  72. Wade, M. J., & Shuster, S. M. (2004). Sexual selection: Harem size and the variance in male reproductive success. American Naturalist, 164(4), E83–E89.PubMedCrossRefGoogle Scholar
  73. Wade, M. J., & Shuster, S. M. (2010). Bateman (1948): Pioneer in the measurement of sexual selection. Heredity, 105(6), 507–508.PubMedCrossRefGoogle Scholar
  74. Weatherhead, P. J., & Boag, P. T. (1995). Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behavioral Ecology and Sociobiology, 37(2), 81–91.CrossRefGoogle Scholar
  75. Weir, L. K., Grant, J. W. A., & Hutchings, J. A. (2011). The influence of operational sex ratio on the intensity of competition for mates. American Naturalist, 177(2), 167–176.PubMedCrossRefGoogle Scholar
  76. Wong, B. B. M., Candolin, U., & Lindström, K. (2007). Environmental deterioration compromises socially-enforced signals of male quality in three-spined sticklebacks. American Naturalist, 170, 184–189.PubMedCrossRefGoogle Scholar
  77. Wootton, R. J. (1973). Effect of size of food ration on egg-production in female 3-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology, 5(1), 89–96.CrossRefGoogle Scholar
  78. Wootton, R. J. (1976) The biology of the sticklebacks: Academic Press.Google Scholar
  79. Wootton, R. J. (1984). The functional biology of sticklebacks. London: Croom Helm.CrossRefGoogle Scholar
  80. Young, K. A., Genner, M. J., Haesler, M. P., & Joyce, D. A. (2010). Sequential female assessment drives complex sexual selection on bower shape in a cichlid fish. Evolution, 64(8), 2246–2253.PubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of BiosciencesUniversity of HelsinkiHelsinkiFinland

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