Evolutionary Biology

, Volume 40, Issue 4, pp 461–470 | Cite as

The “Sex Role” Concept: An Overview and Evaluation

Synthesis Paper

Abstract

“Sex roles” are intuitively associated to stereotypic female and male sexual strategies and in biology, the term “sex role” often relates to mating competition, mate choice or parental care. “Sex role reversals” imply that the usual typological pattern for a population or species is deviates from a norm, and the meaning of “sex role reversal” thus varies depending upon whatever is the usual pattern of sex-typical behavior in a given taxon. We identify several problems with the current use of the “sex role” concept. (1) It is typological and reflects stereotypic expectations of the sexes. (2) The term “sex role” parses continuous variation into only two categories, often obscuring overlap, between the sexes in behavior and morphology, and variability in relation to ecological circumstances. (3) Common generalizations such as “sex role as seen in nature” mask variation upon which selection may act. (4) The general meaning of “sex roles” in society (i.e. “socially and culturally defined prescriptions and beliefs about the behavior and emotions of men and women”) is contrary to biological “sex role” concepts, so that confusing the two obscure science communication in society. We end by questioning the validity of the “sex role” concept in evolutionary biology and recommend replacing the term “sex role” with operational descriptions.

Keywords

Mate choice Mating competition Sex roles Sexual selection Sex role reversal 

Notes

Acknowledgments

We are most grateful for comments on an earlier version of this manuscript from Patricia A. Gowaty and anonymous reviewers, discussions with Lotta Kvarnemo, Patricia A. Gowaty, Marlene Zuk, and participants in the OIKOS 2006 workshop, the 2008 Gender perspectives on sexual selection workshop in Uppsala, and the symposium on the Ecology of sex roles in Perth 2011. MA and IA were supported by the GenNa-program, funded by the Swedish Research Council, at the Centre for Gender Research, Uppsala University. I.A. was also supported by a Grant from the Inez Johansson foundation, and M.A. by a Grant from the Royal Swedish Academy of Sciences.

References

  1. Ah-King, M., & Nylin, S. (2010). Flexible mate choice. In M. D. Breed & J. Moore (Eds.), Encyclopedia of animal behavior. Amsterdam: Elsevier.Google Scholar
  2. Ah-King, M. (2011a). Female sexual selection in light of the Darwin-Bateman paradigm. Behavioral Ecology, 22(6), 1142–1143.CrossRefGoogle Scholar
  3. Ah-King, M. (2011b). Biologins paradox: föränderliga kön och rigida normer. [The paradox of biology: Flexible sexes and rigid norms.] Lambda Nordica, 4, 26–52.Google Scholar
  4. Ah-King, M. (2013). On anisogamy and the evolution of ‘sex-roles’. Trends in Ecology & Evolution, 28(1), 1–2.CrossRefGoogle Scholar
  5. Ah-King, M., & Ahnesjö, I. (2012). Vad kan vi lära av biologisk forskning om “könsroller”? [What can we learn from biological research about “sex roles”?] Tidskrift för genusvetenskap, 4, 51–56.Google Scholar
  6. Ahnesjö, I., Forsgren, E., & Kvarnemo, C. (2008). Variation in sexual selection in fishes. In C. Magnhagen, V. Braithwaite, E. Forsgren, & B. G. Kapoor (Eds.), Fish Behaviour. Enfield: Science Publ. Inc.Google Scholar
  7. Ahnesjö, I., Kvarnemo, C., & Merilaita, S. (2001). Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behavioral Ecology, 12, 397–401.CrossRefGoogle Scholar
  8. Altmann, J. (1997). Mate choice and intrasexual reproductive competition: Contributions to reproduction that go beyond acquiring more mates. In P. A. Gowaty (Ed.), Feminism and evolutionary biology, boundaries, intersections and frontiers (pp. 320–333). New York: Chapman & Hall.Google Scholar
  9. Amundsen, T. (2000). Why are female birds ornamented? Trends in Ecology & Evolution, 15, 149–155.CrossRefGoogle Scholar
  10. Anderson, W. W., Yong-Kyu, K., & Gowaty, P. A. (2007). Experimental constraints on mate preferences in drosophila pseudoobscura decrease offspring viability and fitness of mated pairs. Proceedings of the National Academy of Sciences of the United States of America, 104, 4484–4488.PubMedCrossRefGoogle Scholar
  11. Andersson, M. (1994). Sexual selection. Princeton, New Jersey: Princeton University Press.Google Scholar
  12. Andersson, M. (2005). Evolution of classical polyandry: Three steps to female emancipation. Ethology, 111, 1–23.CrossRefGoogle Scholar
  13. Anselmi, D. L., & Law, A. L. (Eds.). (1998). Questions of gender: Perspectives and paradoxes. Boston: McGraw Hill.Google Scholar
  14. Anthes, N., Putz, A., & Michiels, N. K. (2006). Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: A new framework. Animal Behaviour, 72, 1–12.CrossRefGoogle Scholar
  15. Arnqvist, G., Jones, T. M., & Elgar, M. A. (2007). The extraordinary mating system of Zeus bugs (Heteroptera: Veliidae: Phoreticovelia sp.). Australian Journal of Zoology, 55, 131–137.CrossRefGoogle Scholar
  16. Bailey, N. W., & Zuk, M. (2009). Same-sex sexual behavior and evolution. Trends in Ecology & Evolution, 24, 439–446.CrossRefGoogle Scholar
  17. Barlow, G. W. (2005). How do we decide that a species is sex-role reversed? Quarterly Review of Biology, 80, 28–35.PubMedCrossRefGoogle Scholar
  18. Barreto, F. S., & Avise, J. C. (2010). Quantitative measures of sexual selection reveal no evidence for sex-role reversal in a sea spider with prolonged paternal care. Proceedings of the Royal Society Series B-Biological Sciences, 277, 2951–2956.CrossRefGoogle Scholar
  19. Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2, 349–368.PubMedCrossRefGoogle Scholar
  20. Bonduriansky, R. (2001). The evolution of male mate choice in insects: A synthesis of ideas and evidence. Biological Reviews, 76, 305–339.PubMedCrossRefGoogle Scholar
  21. Bonduriansky, R. (2009). Reappraising sexual coevolution and the sex roles. PLoS Biology, 7, e1000255.PubMedCrossRefGoogle Scholar
  22. Borg, Å., Forsgren, E., & Magnhagen, C. (2002). Plastic sex-roles in the common goby: The effect of nest availability. Oikos, 98, 105–115.CrossRefGoogle Scholar
  23. Bro-Jorgensen, J. (2007). Reversed sexual conflict in a promiscuous antelope. Current Biology, 17, 2157–2161.PubMedCrossRefGoogle Scholar
  24. Clark, A. B. (1978). Sex ratio and local resource competition in a prosimian primate. Science, 201, 163–165.PubMedCrossRefGoogle Scholar
  25. Clutton-Brock, T. (2007). Sexual selection in males and females. Science, 318, 1882–1885.PubMedCrossRefGoogle Scholar
  26. Clutton-Brock, T. (2009). Sexual selection in females. Animal Behaviour, 77, 3–11.CrossRefGoogle Scholar
  27. Clutton-Brock, T. H., Albon, S. D., & Guinness, F. E. (1982). Competition between female relatives in a matrilocal mammal. Nature, 300, 178–180.CrossRefGoogle Scholar
  28. Cunningham, E. J. A., & Birkhead, T. R. (1998). Sex roles and sexual selection. Animal Behaviour, 56, 1311–1321.PubMedCrossRefGoogle Scholar
  29. Darwin, C. (1871). The descent of man and selection in relation to sex. London: John Murray.CrossRefGoogle Scholar
  30. de Jong, K., Wacker, S., Amundsen, T., & Forsgren, E. (2009). Do operational sex ratio and density affect mating behaviour? An experiment on the two-spotted goby. Animal Behaviour, 78, 1229–1238.CrossRefGoogle Scholar
  31. Dewsbury, D. A. (2005). The Darwin-Bateman Paradigm in historical context. Integrative Comparative Biology, 45, 831–837.PubMedCrossRefGoogle Scholar
  32. Edward, D. A., & Chapman, T. (2011). The evolution and significance of male mate choice. Trends in Ecology & Evolution, 26, 647–654.CrossRefGoogle Scholar
  33. Eens, M., & Pinxten, R. (2000). Sex-role reversal in vertebrates: Behavioural and endocrinological accounts. Behavioural Processes, 51, 135–147.PubMedCrossRefGoogle Scholar
  34. Forsgren, E., Amundsen, T., Borg, A. A., & Bjelvenmark, J. (2004). Unusually dynamic sex roles in a fish. Nature, 429, 551–554.PubMedCrossRefGoogle Scholar
  35. Fritzsche, K., Arnqvist, G. (in press). Homage to Bateman: Sex roles predict sex differences in sexual selection. Evolution. doi:  10.1111/evo.12086.
  36. Ganetz, H. (2004). Familiar beasts: Nature, culture and gender in wildlife films on television. Nordicom Review, 25, 197–213.Google Scholar
  37. Gowaty, P. A. (1981). The aggression of breeding easternbluebirds, Sialia sialis, toward each other and intra- and interspecific intruders. Animal Behaviour, 29, 1013–1027.CrossRefGoogle Scholar
  38. Gowaty, P. A. (1982). Sexual terms in sociobiology—Emotionally evocative and paradoxically, jargon. Animal Behaviour, 30, 630–631.CrossRefGoogle Scholar
  39. Gowaty, P. A. (1983). Male parental care and apparent monogamy among eastern bluebirds (Sialia sialis). The American Naturalist, 121(2), 149–157.CrossRefGoogle Scholar
  40. Gowaty, P. A. (1997). Sexual dialectics, sexual selection, and variation in reproductive behavior. In P. A. Gowaty (Ed.), Feminism and evolutionary biology: Boundaries, intersections and frontiers (pp. 351–384). New York: Chapman & Hall.CrossRefGoogle Scholar
  41. Gowaty, P. A. (2011). What is sexual selection and the short herstory of female trait variation. Behavioral Ecology, 22(6), 1146–1147.PubMedCrossRefGoogle Scholar
  42. Gowaty, P. A., Anderson, W. W., Bluhm, C. K., Drickamer, L. C., & Kim, Y. K. (2007). The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proceedings of the National Academy of Sciences of the United States of America, 104, 15023–15027.PubMedCrossRefGoogle Scholar
  43. Gowaty, P. A., & Hubbell, S. P. (2005). Chance, time allocation, and the evolution of adaptively flexible sex role behavior. Integrative and Comparative Biology, 45, 931–944.PubMedCrossRefGoogle Scholar
  44. Gowaty, P. A., & Hubbell, S. P. (2009). Reproductive decisions under ecological constraints: It’s about time. Proceedings of the National Academy of Sciences of the United States of America, 106, 10017–10024.PubMedCrossRefGoogle Scholar
  45. Gowaty, P. A., & Hubbell, S. P. (2013). The evolutionary origins of female mating failures and multiple mating. Entomologia Experimentalis et Applicata, 146(1), 11–25.CrossRefGoogle Scholar
  46. Gowaty, P. A., Kim, Y. K., & Anderson, W. W. (2012). No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster. Proceedings of the National Achademy of Sciences, 109(29), 11740–11745.CrossRefGoogle Scholar
  47. Gowaty, P. A., & Wagner, S. J. (1988). Breeding season aggression of female and male Eastern bluebirds (Sialia sialis) to models of potential conspecific and interspecific egg dumpers. Ethology, 78, 238–250.CrossRefGoogle Scholar
  48. Goymann, W., Wittenzellner, A., & Wingfield, J. C. (2004). Competing females and caring males. Polyandry and sex-role reversal in African black coucals, Centropus grillii. Ethology, 110, 807–823.CrossRefGoogle Scholar
  49. Griffith, S. C., Owens I. P. E., & Thuman, K. A. (2002). Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology, 11, 2195–2212.PubMedCrossRefGoogle Scholar
  50. Gross, M. R., & Sargent, R. C. (1985). The evolution of male and female parental care in fishes. American Zoologist, 25, 807–822.Google Scholar
  51. Gwynne, D. T. (1981). Sexual difference theory—Mormon crickets show role reversal in mate choice. Science, 213, 779–780.PubMedCrossRefGoogle Scholar
  52. Gwynne, D. T., & Simmons, L. W. (1990). Experimental reversal of courtship roles in an insect. Nature, 346, 172–174.CrossRefGoogle Scholar
  53. Hrdy, S. B. (1981). The woman that never evolved. Cambridge: Harvard University Press.Google Scholar
  54. Hrdy, S. B. (1986). Empathy, polyandry and the myth of the coy female. In R. Breed (Ed.), Feminist approaches to science (pp. 119–146). New York: Pergamon Press.Google Scholar
  55. Hunt, J., Breuker, C. J., Sadowski, J. A., & Moore, A. J. (2009). Male-male competition, female mate choice and their interaction: Determining total sexual sexual selection. Journal of Evolutionary Biology, 22, 13–26.PubMedCrossRefGoogle Scholar
  56. Itzkowitz, M., Santangelo, N., & Richter, M. (2001). Parental division of labour and the shift from minimal to maximal role specializations: An examination using a biparental fish. Animal Behaviour, 61, 1237–1245.CrossRefGoogle Scholar
  57. Jiggins, F. M., Hurst, G. D. D., & Majerus, M. E. N. (2000). Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proceedings of the Royal Society Series B-Biological Sciences, 267, 69–73.CrossRefGoogle Scholar
  58. Johnson, L. K. (1982). Sexual selection in a brentid weevil. Evolution, 36, 251–262.CrossRefGoogle Scholar
  59. Jones, A. G., Rosenqvist, G., Berglund, A., & Avise, J. C. (2005). The measurement of sexual selection using Bateman’s principles: An experimental test in the sex-role-reversed pipefish Syngnathus typhle. Integrative and Comparative Biology, 45, 874–884.PubMedCrossRefGoogle Scholar
  60. Jones, A. G., Walker, D., & Avise, J. C. (2001). Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish. Proceedings of the Royal Society Series B-Biological Sciences, 268, 2531–2535.CrossRefGoogle Scholar
  61. Klug, H., Lindström, K., & Kokko, H. (2010). Who to include in measures of sexual selection is no trivial matter. Ecology Letters, 13, 1094–1102.PubMedCrossRefGoogle Scholar
  62. Kokko, H., & Jennions, M. D. (2008). Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21, 919–948.PubMedCrossRefGoogle Scholar
  63. Kosztolanyi, A., Barta, Z., Kupper, C., & Szekely, T. (2011). Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird. Journal of Evolutionary Biology, 24, 1842–1846.PubMedCrossRefGoogle Scholar
  64. Kvarnemo, C., Moore, G. I., & Jones, A. G. (2007). Sexually selected females in the monogamous Western Australian seahorse. Proceedings of the Royal Society Series B-Biological Sciences, 274, 521–525.CrossRefGoogle Scholar
  65. Kvarnemo, C., & Simmons, L. W. (1999). Variance in female quality, operational sex ratio and male mate choice in a bushcricket. Behavioral Ecology and Sociobiology, 45, 245–252.CrossRefGoogle Scholar
  66. Kvarnemo, C., & Simmons, L. W. (2013). Polyandry as a mediator of sexual selection before and after mating. Philosophical Transactions of the Royal Society of London B Biological Sciences, 368, 20120042.CrossRefGoogle Scholar
  67. Lawton, M., Garstka, F., William, R., & Hanks, J. C. (1997). The mask of theory and the face of nature. In P. A. Gowaty (Ed.), Feminism and evolutionary biology: Boundaries, intersections and frontiers (pp. 63–85). New York: Chapman & Hall.CrossRefGoogle Scholar
  68. Lyon, B. E., & Montgomerie, R. (2012). Sexual selection is a form of social selection. Philosophical Transactions of the Royal Society B, 367, 2266–2273.CrossRefGoogle Scholar
  69. Maddison, W. P., Maddison, D. R. (2010). Mesquite: A modular system for evolutionary analysis. Version 2.73 http://mesquiteproject.org.
  70. Mattle, B., & Wilson, A. B. (2009). Body size preferences in the pot-bellied seahorse Hippocampus abdominalis: Choosy males and indiscriminate females. Behavioral Ecology and Sociobiology, 63, 1403–1410.PubMedCrossRefGoogle Scholar
  71. Maurer, G., Double, M. C., Milenkaya, O., Süsser, M., & Magrath, R. D. (2011). Breaking the rules: Sex roles and genetic mating system of the pheasant coucal. Oecologia, 167, 413–425.PubMedCrossRefGoogle Scholar
  72. Myhre, L., de Jong, K., Forsgren, E., & Amundsen, T. (2012). Sex roles and mutual mate choice matter during mate sampling. American Naturalist, 179, 741–755.PubMedCrossRefGoogle Scholar
  73. Owens, I. P. F., Burke, T., & Thompson, D. B. A. (1994). Extraordinary sex-roles in the Eurasian dotterel—Female mating arenas, female-female competition, and female mate choice. American Naturalist, 144, 76–100.CrossRefGoogle Scholar
  74. Parker, G. A., Baker, R. R., & Smith, V. G. F. (1972). The origin and evolution of gamete dimorphism and the male–female phenomenon. Journal of Theoretical Biology, 36, 529–553.PubMedCrossRefGoogle Scholar
  75. Pizzari, T., & Wedell, N. (2013). The polyandry revolution. Philosophical Transactions of the Royal Society of London B Biological Sciences, 368, 20120041.CrossRefGoogle Scholar
  76. Ralls, K. (1976). Mammals in which females are larger than males. The Quarterly Review of Biology, 51(2), 245–276.PubMedCrossRefGoogle Scholar
  77. Rosenqvist, G., & Berglund, A. (2011). Sexual signals and mating patterns in Syngnathidae. Journal of Fish Biology, 78, 1647–1661.PubMedCrossRefGoogle Scholar
  78. Rosvall, K. A. (2011). Intrasexual competition in females: Evidence for sexual selection? Behavioral Ecology, 22, 1131–1140.PubMedCrossRefGoogle Scholar
  79. Rubenstein, D. R. (2012). Sexual and social competition: broadening perspectives by defining female roles: Introduction. Philosophical Transactions of the Royal Society B, 367, 2248–2252.CrossRefGoogle Scholar
  80. Rytkonen, S., Orell, M., & Koivula, K. (1993). Sex-role reversal in willow tit nest defense. Behavioral Ecology and Sociobiology, 33, 275–282.CrossRefGoogle Scholar
  81. Salehialavi, Y., Fritzsche, K., & Arnqvist, G. (2011). The cost of mating and mutual mate choice in two role-reversed seed honey locust beetles. Behavioral Ecology, 22, 1104–1113.CrossRefGoogle Scholar
  82. Schärer, L., Rowe, L., & Arnqvist, G. (2012). Anisogamy, chance and the evolution of sex roles. Trends in Ecology & Evolution, 27, 260–264.CrossRefGoogle Scholar
  83. Shuster, S. M., Briggs, W. R., & Dennis, P. A. (2013). How multiple mating by females affects sexual selection. Philosophical Transactions of the Royal Society B, 367, 20120046.CrossRefGoogle Scholar
  84. Silk, J. B., Clark-Wheatley, C. B., et al. (1981). Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Animal Behaviour, 29, 1106–1120.CrossRefGoogle Scholar
  85. Silva, K., Vieira, M. N., Almada, V. C., & Monteiro, N. M. (2010). Reversing sex role reversal: Compete only when you must. Animal Behaviour, 79, 885–893.CrossRefGoogle Scholar
  86. Small, M. F. (1993). Female choices; Sexual behavior of female primates. Ithaca, NY: Cornell University Press.Google Scholar
  87. Snyder, B. F., & Gowaty, P. A. (2007). A reappraisal of Bateman’s classic study of intrasexual selection. Evolution, 61, 2457–2468.PubMedCrossRefGoogle Scholar
  88. Stockley, P., & Bro-Jorgensen, J. (2011). Female competition and its evolutionary consequences in mammals. Biological Reviews, 86, 341–366.PubMedCrossRefGoogle Scholar
  89. Sutherland, W. J. (1985). Chance can produce a sex difference in variance in mating success and account for Bateman’s data. Animal Behaviour, 33, 1349–1352.CrossRefGoogle Scholar
  90. Svensson, B. G., & Petersson, E. (2000). Swarm site fidelity in the sex role-reversed dance fly Empis borealis. Journal of Insect Behavior, 13, 785–796.CrossRefGoogle Scholar
  91. Tang-Martinez, Z. (2010). Bateman’s principles: Original experiment and modern data for and against. In M. D. Breed & J. Moore (Eds.), Encyclopedia of animal behavior. Amsterdam: Elsevier.Google Scholar
  92. Tang-Martinez, Z., & Ryder, T. B. (2005). The problem with paradigms: Bateman’s worldview as a case study. Integrative and Comparative Biology, 45, 821–830.PubMedCrossRefGoogle Scholar
  93. Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 136–179). Chicago: Aldine.Google Scholar
  94. Ursprung, E., Ringler, M., Jehle, R., & Hödl, W. (2011). Strong male-male competition allows for nonchoosy females: High levels of polygynandry in a territorial frog with paternal care. Molecular Ecology, 20, 1759–1771.PubMedCrossRefGoogle Scholar
  95. Vincent, A., Ahnesjö, I., Berglund, A., & Rosenqvist, G. (1992). Pipefishes and seahorses—Are they all sex-role reversed? Trends in Ecology & Evolution, 7, 237–241.CrossRefGoogle Scholar
  96. West, C., & Zimmerman, D. H. (1987). Doing gender. Gender & Society, 1, 125–151.CrossRefGoogle Scholar
  97. Williams, G. C. (1966). Adaptation and natural selection. Princeton: Princeton University Press.Google Scholar
  98. Williams, G. C. (1975). Sex and evolution. Princeton, NJ: Princeton University Press.Google Scholar
  99. Wilson, A. B., Ahnesjö, I., Vincent, A. C. J., & Meyer, A. (2003). The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae). Evolution, 57, 1374–1386.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Centre for Gender ResearchUppsala UniversityUppsalaSweden
  2. 2.Department of Ecology and Genetics/Animal EcologyUppsala UniversityUppsalaSweden

Personalised recommendations