Breaking the parthenogenesis fertilization barrier: direct and indirect selection pressures promote male fertilization of parthenogenetic females

Abstract

All else being equal, females would double their fecundity through parthenogenetic reproduction. On the other hand, males should be subject to positive selection pressures to coerce parthenogenetic females into sexual fertilization, because the twofold advantage of parthenogenesis is achieved at the expense of the male genetic contribution. Interestingly, although male coercion superficially imposes the cost of sex on parthenogenetic females, it would confer a reproductive benefit even on the parthenogens. This is because females fertilized by coercive males gain indirect reproductive success via sons inheriting coercion, who would succeed in mating with other parthenogens in the next generation (sons’ effect). In this study, using two mathematical models, I show for the first time that the indirect sons’ effect of male coercion plays an important role in the maintenance of sex in potentially parthenogenetic species. The first model, which compares the fitness of a female reproducing parthenogenetically with that of a female mating with a coercive male, demonstrates that the sons’ effect can outweigh the cost of sex and resolve sexual conflict over reproductive modes. My second model of population genetics, which analyses the dynamics of coercion and parthenogenesis, shows that the occurrence of parthenogenetic reproduction is suppressed in the presence of the sons’ effect of male coercion. These results indicate that the sons’ effect of male coercion helps to maintain sexual reproduction at an evolutionary time scale, as well as offset the twofold cost of males in the invasion phase of the coercion.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Andrès JA, Morrow EH (2003) The origin of interlocus sexual conflict: is sex-linkage important? J Evol Biol 16:219–223

    PubMed  Article  Google Scholar 

  2. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton

  3. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, Berkley

    Google Scholar 

  4. Cameron ET, Rowe L (2003) Sexual conflict and indirect benefits. J Evol Biol 16:1055–1060

    CAS  PubMed  Article  Google Scholar 

  5. Chapman T, Arnqvist J, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47

    Article  Google Scholar 

  6. Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56

    Article  Google Scholar 

  7. Conallon TR, Cox M, Calsbeek R (2009) Fitness consequences of sex-specific selection. Evolution 64:1671–1682

    Article  Google Scholar 

  8. Corley LS, Moore AJ (1999) Fitness of alternative modes of reproduction: developmental constraints and the evolutionary maintenance of sex. Proc R Soc Lond B 266:471–476

    Article  Google Scholar 

  9. Dagg JL (2006) Could sex be maintained through harmful males? Oikos 112:232–235

  10. D’Souza TG, Michiels NK (2010) The costs and benefits of occasional sex: theoretical predictions and a case study. J Hered 101:S34–S41

    PubMed  Article  Google Scholar 

  11. Engelstädter J (2008) Constraints on the evolution of sexual reproduction. BioEssays 30:1138–1150

    PubMed  Article  Google Scholar 

  12. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

  13. Gavrilets S (2000) Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886–889

    CAS  PubMed  Article  Google Scholar 

  14. Gavrilets S, Arnqvist G, Fibers U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc B 268:531–539

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  15. Godfray HCJ (1995) Evolutionary theory of parent-offspring conflict. Nature 376:1133–1138

    Article  Google Scholar 

  16. Greeen RF, Noakes DLG (1995) Is a little bit of sex as good as a lot? J Theor Biol 174:87–96

    Article  Google Scholar 

  17. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290

    Article  Google Scholar 

  18. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites. Proc Natl Acad Sci USA 87:3566–3573

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Hurst LD, Peck JR (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol Evol 11:46–52

    CAS  PubMed  Article  Google Scholar 

  20. Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences. II. The “handicap” principle. Evolution 45:1431–1442

    Article  Google Scholar 

  21. Jennions MD, Kokko H (2010) Sexual selection. In: Westneat DF, Fox CW (eds) Evolutionary behavioral ecology. Oxford University Press, Oxford, pp 343–364

    Google Scholar 

  22. Kawatsu K (2013a) Sexually antagonistic coevolution for sexual harassment can act as a barrier to further invasions by parthenogenesis. Am Nat 181:223–234

    PubMed  Article  Google Scholar 

  23. Kawatsu K (2013b) Sexual conflict over the maintenance of sex: effects of sexually antagonistic coevolution for reproductive isolation of parthenogenesis. PLoS ONE 8:e58141

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. Keightley PD, Eyre-Walker A (2000) Deleterious mutations and the evolution of sex. Science 290:331–333

    CAS  PubMed  Article  Google Scholar 

  25. Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution 36:1–12

    Article  Google Scholar 

  26. Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–440

    CAS  PubMed  Article  Google Scholar 

  27. Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:435–441

    Google Scholar 

  28. Kramer MG, Templeton AR, Miller KG (2002) Evolutionary implications of developmental instability in parthenogenetic Drosophila mercatorum. I. comparison of several strains with different genotypes. Evol Dev 4:223–233

    PubMed  Article  Google Scholar 

  29. Lamatsch DK, Stöck M (2009) Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. In: Schön I, Martens K, van Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, New York, pp 399–432

    Google Scholar 

  30. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–307

    Article  Google Scholar 

  31. Lehtonen J, Jennions MD, Kokko H (2012) The many costs of sex. Trends Ecol Evol 27:172–178. doi:10.1016/j.tree.2011.09.016

    PubMed  Article  Google Scholar 

  32. Matsuura K, Nishida T (2001) Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul Ecol 43:119–124

    Article  Google Scholar 

  33. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge

    Google Scholar 

  34. Otto SP, Nuismer SL (2004) Species interactions and the evolution of sex. Science 304:1018–1020

    CAS  PubMed  Article  Google Scholar 

  35. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, London, pp 123–166

    Google Scholar 

  36. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc B 61:235–259

    Article  Google Scholar 

  37. Rankin DJ (2008) Can punishment maintain sex? Oikos 117:173–176

  38. Rice WR, Holland B (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav Ecol Sociobiol 18:922–929

    Google Scholar 

  39. Scali V (2009) Metasexual stick insects: model pathways to losing sex and bringing it back. In: Schön I, Martens K, van Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, New York, pp 317–345

    Google Scholar 

  40. Schwander T, Vuilleumier S, Dubman J, Crespi BJ (2010) Positive feedback in the transition from sexual reproduction to parthenogenesis. Proc R Soc B 277:1435–1442

    PubMed Central  PubMed  Article  Google Scholar 

  41. Simon JC, Delmotte F, Rispe C, Crease T (2003) Phylogenetic relationship between parthenogenesis and their sexual relatives: the possible route to parthenogenesis in animals. Biol J Linn Soc 79:151–163

    Article  Google Scholar 

  42. West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12:1003–1012

  43. Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

    Google Scholar 

Download references

Acknowledgments

I thank Dr. Kenji Fujisaki for help with this study. I also thank two anonymous reviewers for helpful discussions. This work was supported by Research Fellowships for Young Scientists awarded by the Japan Society for the Promotion of Science (JSPS).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kazutaka Kawatsu.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kawatsu, K. Breaking the parthenogenesis fertilization barrier: direct and indirect selection pressures promote male fertilization of parthenogenetic females. Evol Ecol 29, 49–61 (2015). https://doi.org/10.1007/s10682-014-9749-0

Download citation

Keywords

  • Maintenance of sex
  • Sexual conflict
  • Sons’ effect
  • Facultative parthenogenesis
  • Battleground analysis
  • Population genetics