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Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity

Abstract

Postcopulatory sperm competition is a key aspect of sexual selection and is believed to drive the rapid evolution of both reproductive physiology and reproduction-related genes1,2,3,4. It is well-established that mating behavior determines the intensity of sperm competition, with polyandry (i.e., female promiscuity) leading to fiercer sperm competition than monandry1,2,3. Studies in mammals, particularly primates, showed that, owing to greater sperm competition, polyandrous taxa generally have physiological traits that make them better adapted for fertilization than monandrous species, including bigger testes, larger seminal vesicles, higher sperm counts, richer mitochondrial loading in sperm and more prominent semen coagulation2,5,6,7,8. Here, we show that the degree of polyandry can also impact the dynamics of molecular evolution. Specifically, we show that the evolution of SEMG2, the gene encoding semenogelin II, a main structural component of semen coagulum, is accelerated in polyandrous primates relative to monandrous primates. Our study showcases the intimate relationship between sexual selection and the molecular evolution of reproductive genes.

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Figure 1: Lineage-specific ω values of SEMG2 in primates, calculated using the SEMG2 coding region before the stop codon present in the chimpanzees, which occurs earlier than in the other primates17.
Figure 2: Correlation between the rate of evolution of SEMG2 and reproductive behavior and physiology in primates.
Figure 3: Sliding-window analysis of ω values in the common chimpanzee lineage and the crab-eating macaque lineage.

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References

  1. Karr, T.L. & Pitnick, S. Sperm competition: defining the rules of engagement. Curr. Biol. 9, R787–R790 (1999).

    CAS  Article  Google Scholar 

  2. Dixson, A. & Anderson, M. Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings. Annu. Rev. Sex Res. 12, 121–144 (2001).

    CAS  PubMed  Google Scholar 

  3. Birkhead, T.R. & Pizzari, T. Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262–273 (2002).

    CAS  Article  Google Scholar 

  4. Swanson, W.J. & Vacquier, V.D. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137–144 (2002).

    CAS  Article  Google Scholar 

  5. Harcourt, A.H., Harvey, P.H., Larson, S.G. & Short, R.V. Testis weight, body weight and breeding system in primates. Nature 293, 55–57 (1981).

    CAS  Article  Google Scholar 

  6. Dixson, A.F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Being (Oxford University Press, New York, 1998).

    Google Scholar 

  7. Dixson, A.L. & Anderson, M.J. Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol. (Basel) 73, 63–69 (2002).

    Article  Google Scholar 

  8. Anderson, M.J. & Dixson, A.F. Sperm competition: motility and the midpiece in primates. Nature 416, 496 (2002).

    CAS  Article  Google Scholar 

  9. Voss, R. Male accessory glands and the evolution of copulatory plugs in rodents. Occ. Pap. Mus. Zool. Univ. Mich. 689, 1–17 (1979).

    Google Scholar 

  10. Kingan, S.B., Tatar, M. & Rand, D.M. Reduced polymorphism in the chimpanzee semen coagulating protein, semenogelin I. J. Mol. Evol. 57, 159–169 (2003).

    CAS  Article  Google Scholar 

  11. Dewsbury, D.A. A test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus). J. Mammal. 69, 854 (1988).

    Article  Google Scholar 

  12. Michener, G.R. Copulatory plugs in Richardson's ground squirrels. Can. J. Zool. 62, 267–270 (1984).

    Article  Google Scholar 

  13. Blandau, R.J. On factors involved in sperm transport through the cervix uteri of the albino rat. Am. J. Anat. 73, 253–272 (1945).

    Article  Google Scholar 

  14. Mathews, M.K. & Adler, N.T. Systematic interrelationships of mating, vaginal plug position, and sperm transport in the rat. Physiol. Behav. 20, 303–309 (1978).

    Article  Google Scholar 

  15. Dunbar, R.I. & Dunbar, E.P. Contrasts in social structure among black-and-white colobus monkey groups. Anim. Behav. 24, 84–92 (1976).

    CAS  Article  Google Scholar 

  16. Rodman, P.S. & Mitani, J.C. Orang-utans: sexual dimorhism in a solitary species in Primate Societies (eds. Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R. & Struhsaker, T.) 146–154 (University of Chicago Press, Chicago, 1987).

  17. Jensen-Seaman, M.I. & Li, W.H. Evolution of the hominoid semenogelin genes, the major proteins of ejaculated semen. J. Mol. Evol. 57, 261–270 (2003).

    CAS  Article  Google Scholar 

  18. Yang, Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15, 568–573 (1998).

    CAS  Article  Google Scholar 

  19. Nielsen, R. & Yang, Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929–936 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Conoway, C.H. & Koford, C.B. Estrous cycles and mating behavior in a free-ranging band of rhesus monkey. J. Mammal. 45, 577–588 (1965).

    Article  Google Scholar 

  21. Tokuda, K., Simms, R.C. & Jenson, J.D. Sexual behavior in a captive group of pigtail macaque (Macaca nemestrina). Primates 9, 283–294 (1968).

    Article  Google Scholar 

  22. Van Noordwijk, M.A. Sexual behavior of Sumatran long-tailed macaques (Macaca fascicularis). Z. Tierpsychol. 70, 277–296 (1985).

    Article  Google Scholar 

  23. Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Harvard University Press, Cambridge, 1986).

    Google Scholar 

  24. Hasegawa, T. & Hiraiwai-Hasegawa, M. Sperm Competition and mating behavior. in The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies (ed. Nishida, T.) 115–132 University of Tokyo Press, Tokyo, 1990.

    Google Scholar 

  25. Manson, J.H. Mating patterns, mate choice and birth season heterosexual relationships in free-ranging rhesus macaques. Primates 35, 417–433 (1992).

    Article  Google Scholar 

  26. Strier, K.B. Faces in the Forest, the Endangered Muriqui Monkeys of Brazil (Oxford University Press, New York, 1992).

    Google Scholar 

  27. Robert, M. & Gagnon, C. Purification and characterization of the active precursor of a human sperm motility inhibitor secreted by the seminal vesicles: identity with semenogelin. Biol. Reprod. 55, 813–821 (1996).

    CAS  Article  Google Scholar 

  28. Lilja, H., Oldbring, J., Rannevik, G. & Laurell, C.B. Seminal vesicle-secreted proteins and their reactions during gelation and liquefaction of human semen. J. Clin. Invest. 80, 281–285 (1987).

    CAS  Article  Google Scholar 

  29. Yang, Z. & Nielsen, R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32–43 (2000).

    CAS  Article  Google Scholar 

  30. Li, W.H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36, 96–99 (1993).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank W.-H. Huang for technical assistance; A. Di Rienzo, C. Malcom, N. M. Pearson, E. J. Vallender and C.-I Wu for discussions and comments on the manuscript; and L.G. Chemnick, A.R. Ryder and L. Faust for providing primate tissue samples. This work was supported in part by the William Rainey Harper Fellowship (to S.D.) and the Searle Scholarship and the Burroughs Wellcome Career Award (to B.T.L.).

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Correspondence to Bruce T Lahn.

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Supplementary information

Supplementary Fig. 1

Lineage-specific ω values of SEMG2 in primates. (PDF 9 kb)

Supplementary Fig. 2

Correlation between the evolutionary rate of SEMG2 and the reproductive behavior/physiology in primates. (PDF 13 kb)

Supplementary Table 1

Likelihood estimates of different evolutionary models. (PDF 9 kb)

Supplementary Table 2

Likelihood ratio between different evolutionary models. (PDF 8 kb)

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Dorus, S., Evans, P., Wyckoff, G. et al. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat Genet 36, 1326–1329 (2004). https://doi.org/10.1038/ng1471

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