Evolutionary Ecology

, Volume 29, Issue 1, pp 49–61 | Cite as

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

  • Kazutaka KawatsuEmail author
Original Paper


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.


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



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).


  1. Andrès JA, Morrow EH (2003) The origin of interlocus sexual conflict: is sex-linkage important? J Evol Biol 16:219–223PubMedCrossRefGoogle Scholar
  2. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  3. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, BerkleyGoogle Scholar
  4. Cameron ET, Rowe L (2003) Sexual conflict and indirect benefits. J Evol Biol 16:1055–1060PubMedCrossRefGoogle Scholar
  5. Chapman T, Arnqvist J, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  6. Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56CrossRefGoogle Scholar
  7. Conallon TR, Cox M, Calsbeek R (2009) Fitness consequences of sex-specific selection. Evolution 64:1671–1682CrossRefGoogle 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 266:471–476CrossRefGoogle Scholar
  9. Dagg JL (2006) Could sex be maintained through harmful males? Oikos 112:232–235Google Scholar
  10. D’Souza TG, Michiels NK (2010) The costs and benefits of occasional sex: theoretical predictions and a case study. J Hered 101:S34–S41PubMedCrossRefGoogle Scholar
  11. Engelstädter J (2008) Constraints on the evolution of sexual reproduction. BioEssays 30:1138–1150PubMedCrossRefGoogle Scholar
  12. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  13. Gavrilets S (2000) Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886–889PubMedCrossRefGoogle Scholar
  14. Gavrilets S, Arnqvist G, Fibers U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc B 268:531–539PubMedCentralPubMedCrossRefGoogle Scholar
  15. Godfray HCJ (1995) Evolutionary theory of parent-offspring conflict. Nature 376:1133–1138CrossRefGoogle Scholar
  16. Greeen RF, Noakes DLG (1995) Is a little bit of sex as good as a lot? J Theor Biol 174:87–96CrossRefGoogle Scholar
  17. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290CrossRefGoogle Scholar
  18. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites. Proc Natl Acad Sci USA 87:3566–3573PubMedCentralPubMedCrossRefGoogle Scholar
  19. Hurst LD, Peck JR (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol Evol 11:46–52PubMedCrossRefGoogle Scholar
  20. Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences. II. The “handicap” principle. Evolution 45:1431–1442CrossRefGoogle Scholar
  21. Jennions MD, Kokko H (2010) Sexual selection. In: Westneat DF, Fox CW (eds) Evolutionary behavioral ecology. Oxford University Press, Oxford, pp 343–364Google Scholar
  22. Kawatsu K (2013a) Sexually antagonistic coevolution for sexual harassment can act as a barrier to further invasions by parthenogenesis. Am Nat 181:223–234PubMedCrossRefGoogle 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:e58141PubMedCentralPubMedCrossRefGoogle Scholar
  24. Keightley PD, Eyre-Walker A (2000) Deleterious mutations and the evolution of sex. Science 290:331–333PubMedCrossRefGoogle Scholar
  25. Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution 36:1–12CrossRefGoogle Scholar
  26. Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–440PubMedCrossRefGoogle Scholar
  27. Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:435–441Google 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 4:223–233PubMedCrossRefGoogle 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 399–432CrossRefGoogle Scholar
  30. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–307CrossRefGoogle 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 PubMedCrossRefGoogle 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 43:119–124CrossRefGoogle Scholar
  33. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  34. Otto SP, Nuismer SL (2004) Species interactions and the evolution of sex. Science 304:1018–1020PubMedCrossRefGoogle 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 123–166CrossRefGoogle Scholar
  36. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc B 61:235–259CrossRefGoogle Scholar
  37. Rankin DJ (2008) Can punishment maintain sex? Oikos 117:173–176Google Scholar
  38. Rice WR, Holland B (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav Ecol Sociobiol 18:922–929Google 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 317–345CrossRefGoogle 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 277:1435–1442PubMedCentralPubMedCrossRefGoogle 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 79:151–163CrossRefGoogle Scholar
  42. West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12:1003–1012Google Scholar
  43. Williams GC (1975) Sex and evolution. Princeton University Press, PrincetonGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of Environmental Solution Technology, Faculty of Science and TechnologyRyukoku UniversityOtsuJapan

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