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Genetic interaction between male mating strategy and sex ratio in a marine isopod

Nature volume 388, pages 373–377 (1997)Cite this article

Abstract

Individual males in many animal species exhibit discrete modes of behaviour1,2,3, but the genetic mechanisms underlying these differences are poorly understood. Here we investigate the genetics of the isopod crustacean Paracerceis sculpta, in which three different types of males coexist, each distinguishable from the others by their behavioural and morphological phenotypes4,5. Within families, alleles of the gene encoding the enzyme phosphoglucomutase (Pgm gene) are associated with particular male phenotypes, although no significant association between these characters exists population-wide. This suggests that Pgm is closely linked to a single genetic locus which controls male phenotype. We call this the alternative mating strategy (Ams) locus. We present evidence that two other factors—an autosomal gene, transformer (Tfr), and an extrachromosomal factor—interact with primary sex determination loci and with alleles at Ams, causing certain individuals to change sex, thereby biasing family sex ratios. A model based on our genetic analysis suggests that: first, polymorphism in male behaviour is controlled by the mendelian segregation of three alleles at the Ams locus; second, that family sex ratio is influenced by alternative alleles at the Tfr locus whose expression is influenced by the extrachromosomal factor; and third, that Tfr and Ams interact epistatically to determine the sex of the individual and, if male, its behaviour and external morphology.

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Figure 1
Figure 2: Effects of Tfr and ECF on Ams and primary sex determination loci: α, β, γ are alleles at Ams; M, male; F, female; Tfri represent alleles at Tfr; minus sign, no effect of Tfr on Ams-sex combination; plus sign, sex change, with an arrow indicating the direction of change; asterisk, effect produced by interaction of ECF with Tfr, Ams and primary sex-determination genotypes.
Figure 3

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References

  1. Lank, D. B., Smith, C. M., Hanotte, O., Burke, T. & Cooke, F. Genetic polymorphism for alternative mating behaviour in lekking male ruff. Nature 378, 59–62 (1995).

    Article  ADS  CAS  Google Scholar 

  2. Gross, M. R. Alternative reproductive strategies and tactics; diversity within sexes. Trends Ecol. Evol. 11, 92–97 (1996).

    Article  CAS  Google Scholar 

  3. Sinervo, B. & Lively, C. M. The rock–paper–scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996).

    Article  ADS  CAS  Google Scholar 

  4. Shuster, S. M. Alternative reproductive behaviors: Three discrete male morphs in Paracerceis sculpta, an intertidal isopod from the northern Gulf of California. J. Crust. Biol. 7, 318–327 (1987).

    Article  Google Scholar 

  5. Shuster, S. M. The reproductive behaviour of α-, β-, and γ-males in Paracerceis sculpta, a marine isopod crustacean. Behaviour 121, 231–258 (1992).

    Article  Google Scholar 

  6. Shuster, S. M. Male alternative reproductive behaviors in a marine isopod crustacean (Paracerceis sculpta): The use of genetic markers to measure differences in fertilization success among α-, β- and γ-males. Evolution 34, 1683–1698 (1989).

    Google Scholar 

  7. Shuster, S. M. & Wade, M. J. Equal mating success among male reproductive strategies in a marine isopod. Nature 350, 606–61 (1991).

    Article  ADS  Google Scholar 

  8. Sassaman, C. Inbreeding and sex ratio variation in female-biased populations of a clam shrimp, Eulimnadia texana. Bull. Mar. Sci. 45, 425–432 (1989).

    Google Scholar 

  9. Hartl, R. & Clark, A. in Principles of Population Genetics2nd edn, 47–57 (Sinauer, Sunderland, MA, (1989)).

    Google Scholar 

  10. Heath, D. J. & Ratford, J. R. The inheritance of sex ratio in the isopod, Sphaeroma rugicauda. Heredity 64, 419–425 (1990).

    Article  Google Scholar 

  11. Bull, J. J. Evolution of Sex Determining Mechanisms(Benjamin-Cummings, Menlo Park, CA, (1983)).

    Google Scholar 

  12. Legrand, J. J., Legrand-Hamelin, E. & Juchault, P. Sex determination in Crustacea. Biol. Rev. 62, 439–470 (1987).

    Article  Google Scholar 

  13. Juchault, P., Rigaud, T. & Mocquard, J. -P. Evolution of sex-determining mechanisms in a wild population of Armadillidium vulgare Latr. (Crustacea: Isopoda): competition between two feminizing parasitic sex factors. Heredity 69, 382–390 (1992).

    Article  Google Scholar 

  14. Rousset, F., Bouchon, D., Pintureau, B., Juchault, P. & Solignac, M. Wolbachia endosymbionts responsible for various alterations of sexuality in Arthropods. Proc. R. Soc. Lond. B 250, 91–98 (1991).

    ADS  Google Scholar 

  15. Hurst, L. D. The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biol. Rev. 68, 121–193 (1993).

    Article  Google Scholar 

  16. Rigaud, T. & Juchault, P. Conflict between feminizing sex ratio distorters and an autosomal masculinizing gene in the terrestrial isopod, Armadillidium vulgareLatr. Genetics 133, 247–252 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Juchault, P. & Rigaud, T. Evidence for female heterogamety in two terrestrial crustaceans and the problem of sex chromosome evolution in isopods. Heredity 75, 488–471 (1995).

    Article  Google Scholar 

  18. Read, T. R. C. & Cressie, N. A. C. in Goodness-of-fit Statistics for Discrete Multivariate Data 136–139 (Springer, New York, (1988)).

    Book  Google Scholar 

  19. Shuster, S. M. & Wade, M. J. Female copying and sexual selection in a marine isopod crustacean. Anim. Behav. 42, 1071–1078 (1991).

    Article  Google Scholar 

  20. Shuster, S. M. in Crustacean Sexual Biology(eds Bauer, R. T. & Martin, J. W.) 91–110 (Columbia Univ. Press, New York, (1991)).

    Google Scholar 

  21. Levins, R. Evolution in Changing Environments(Princeton Univ. Press, Princeton, (1968)).

    Google Scholar 

  22. Slatkin, M. On the equilibration of fitnesses by natural selection. Am. Nat. 112, 845–859 (1978).

    Article  Google Scholar 

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

    Book  Google Scholar 

  24. Lively, C. M. Canalization versus developmental conversion in a spatially variable environment. Am. Nat. 128, 561–572 (1986).

    Article  Google Scholar 

  25. Slatkin, M. The evolutionary response to frequency and density dependent interactions. Am. Nat. 114, 384–398 (1979).

    Article  MathSciNet  Google Scholar 

  26. Wright, S. Evolution and Genetics of Populations Vol. 2(Univ. of Chicago Press(1969)).

    Google Scholar 

  27. Wade, M. J., Shuster, S. M. & Stevens, L. Bottlenecks, founder events and inbreeding: Experimental studies of the response to selection with Tribolium. Evolution 50, 723–733 (1996).

    Article  Google Scholar 

  28. Shuster, S. M. Changes in female anatomy associated with the reproductive molt in Paracerceis sculpta (Holmes), a semelparous isopod crustacean. J. Zool. 225, 365–379 (1991).

    Article  Google Scholar 

  29. Shuster, S. M. Courtship and female mate selection in a semelparous isopod crustacean (Paracerceis sculpta). Anim. Behav. 40, 390–399 (1990).

    Article  Google Scholar 

  30. Tinturier-Hamelin, E. Sur le polychromatisme de l'isopode Flabellifere Dynamene bidentata (Adams) II. Etude genetique du mutant bimaculata partiellement. Cah. Biol. Mar. 4, 473–591 (1967).

    Google Scholar 

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Acknowledgements

This research was supported by the NSF and by organized research and departmental funding from Northern Arizona University, and was authorized by the Mexican Government. We thank M. Wade and B. Charlesworth for reviewing data and earlier drafts of the manuscript; Y. Toquenaga for statistical advice and for a program for calculating exact χ2 tests; D. Dorado, S. Juarez, S. Hag, H. Baitoo, S. Bhakta, Y. Bhakta, S. Brekhus; H. Yoon; N. Kim, M. Kim, U. Rao and L. Lynch for assistance in maintaining laboratory animals; and V. Jormalainen, P. Nelson, K.Johnson, G. Davis and M. Pitts for discussion.

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  1. *Department of Biological Sciences, Northern Arizona University, Flagstaff, 86011-5640, Arizona, USA

    Stephen M. Shuster

  2. †Department of Biology, University of California, Riverside, 92521, California, USA

    Clay Sassaman

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Shuster, S., Sassaman, C. Genetic interaction between male mating strategy and sex ratio in a marine isopod. Nature 388, 373–377 (1997). https://doi.org/10.1038/41089

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