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Non-fisherian sex ratios with sex change and environmental sex determination

Abstract

FISHER'S theory of sex-ratio evolution1 explains why 1:1 sex ratios are so prevalent2–8. Recent work has therefore emphasized situations in which biased sex ratios tend to evolve (for example, local mate competition7, non-mendelian inheritance of sex-ratio factors7,9,10, haplodiploid social insects11,12 and others6,13). In species where individuals change sex during their adult lifetimes, and in species where sex is determined by environmental conditions experienced during pre-adult development, biased sex ratios are expected and frequently observed6. Sex-ratio models for particular kinds of sex change (SC) and environmental sex determination (ESD) have predicted excesses of the first sex6,14,15 under SC, and of the sex developing in the 'worse' environment under ESD6,14–16. Here we generalize and unite these results in a single model that applies to a wide range of SC and ESD biologies. The principle that emerges from this model appears to explain strong female and male excesses seen in sex-changing fish and invertebrates and in nematodes with ESD. It is not known whether the female excess commonly seen in reptiles with ESD are also explained by this principle.

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References

  1. Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, 1930).

    Book  Google Scholar 

  2. Maynard Smith, J. Evolution and the Theory of Games (Cambridge Univ. Press, Cambridge, 1982).

    Book  Google Scholar 

  3. Shaw, R. F. & Mohler, J. D. Am. Nat. 87, 337–342 (1953).

    Article  Google Scholar 

  4. Williams, G. C. Adaptation and Natural Selection (Princeton Univ. Press, Princeton, 1966).

    Google Scholar 

  5. Leigh, E. G. Oxford Surveys evol. Biol. 3, 187–223 (1986).

    Google Scholar 

  6. Charnov, E. L. The Theory of Sex Allocation (Princeton Univ. Press, Princeton, 1982).

    Google Scholar 

  7. Hamilton, W. D. Science 156, 477–488 (1967).

    Article  ADS  CAS  Google Scholar 

  8. Bull, J. J. & Charnov, E. L. Oxford Surveys evol. Biol. 5, 96–135 (1988).

    Google Scholar 

  9. Lewis, D. New Phytologist 40, 56–63 (1941).

    Article  Google Scholar 

  10. Howard, H. W. J. Genet 44, 143–159 (1942).

    Article  Google Scholar 

  11. Hamilton, W. D. A. Rev. Ecol. Syst 3, 193–232 (1972).

    Article  Google Scholar 

  12. Trivers, R. L. & Hare, H. H. Science 191, 249–263 (1976).

    Article  ADS  CAS  Google Scholar 

  13. Karlin, S. & Lessard, S. Theoretical Studies on Sex Ratio Evolution (Princeton Univ. Press, Princeton, 1986).

    Google Scholar 

  14. Frank, S. A. & Swingland, I. S. J. theor. Biol. 135, 415–418 (1988).

    Article  CAS  Google Scholar 

  15. Charnov, E. L. & Bull, J. J. J. theor. Biol. (in the press).

  16. Bull, J. J. Heredity 46, 9–26 (1981).

    Article  Google Scholar 

  17. Warner, R. R. Environmental Biology of Fishes Vol. 22, 81–90 (1988).

    Article  Google Scholar 

  18. Warner, R. R. Trends Ecol. Evol. 3, 133–136 (1988).

    Article  CAS  Google Scholar 

  19. Shapiro, D. Y. Science 209, 1136–1137 (1980).

    Article  ADS  CAS  Google Scholar 

  20. Trivers, R. L. & Willard, D. E. Science 179, 90–92 (1973).

    Article  ADS  CAS  Google Scholar 

  21. Bull, J. J. Evolution of Sex Determining Mechanisms (Benjamin/Cummings, Menlo Park, 1983).

    Google Scholar 

  22. Blackmore, M. S. thesis, Univ. Utah (1989).

  23. Charnov, E. L. Am. Nat. 113, 715–734 (1979).

    Article  MathSciNet  Google Scholar 

  24. Charnov, E. L., Gotshall, D. & Robinson, J. Science 200, 204–206 (1978).

    Article  ADS  CAS  Google Scholar 

  25. Ballantine, W. J. thesis, London Univ, (1961).

  26. Hoagland, K. E. Malacologia 17, 365–391 (1978).

    Google Scholar 

  27. Robertson, D. R. & Warner, R. R. Smithsonian Contrib. Zool. 255, 1–26 (1978).

    Article  Google Scholar 

  28. Choat, J. H. & Robertson, D. R. in Intersexuality in the Animal Kingdom (ed. Reinboth, R.) 263–283 (Springer, Berlin, 1975).

    Book  Google Scholar 

  29. Warner, R. R. & Robertson, D. R. Smithsonian Contrib. Zool. 254, 1–27 (1978).

    Article  Google Scholar 

  30. Robertson, D. R. & Choat, J. H. Proc. Second Int. Symp. Coral Reefs 1 (Biology), 217–225 (1974).

    Google Scholar 

  31. Moe, M. A. Florida Dept. Nat. Resources Prof. Paper 10, 1–95 (1969).

    Google Scholar 

  32. Shapiro, D. Y. & Lubbock, R. J. theor. Biol. 82, 411–426 (1980).

    Article  Google Scholar 

  33. Fricke, H. & Fricke, S. Nature 266, 830–832 (1977).

    Article  ADS  CAS  Google Scholar 

  34. Fricke, H. W. Z. Tierpsychol. 50, 313–326 (1979).

    Article  Google Scholar 

  35. Moyer, J. T. & Nakazono, A. Jap. J. Ich. 25, 25–39 (1978).

    Google Scholar 

Download references

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Charnov, E., Bull, J. Non-fisherian sex ratios with sex change and environmental sex determination. Nature 338, 148–150 (1989). https://doi.org/10.1038/338148a0

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