Evolutionary Biology

, Volume 39, Issue 2, pp 271–281 | Cite as

Stochasticity in Sexual Selection Enables Divergence: Implications for Moth Pheromone Evolution

  • Elizabeth L. Bergen
  • Jonathan T. Rowell
  • Fred Gould
  • Maria R. ServedioEmail author
Research Article


Sexual selection has long been hypothesized to lead to allopatric speciation, and one possible mechanism for this is that its interaction with stochasticity, which perturbs the trait and preference equilibria, can result in different traits being preferred in different populations. Here we specifically examine the role that stochastic changes in sexual selection strength plays in the shift of predominance between pairs of preferences and traits within a single population. We first create a single-locus null model of stochasticity during frequency dependent selection and then compare it to a two-locus population genetic model with stochastic strengths of female preferences for male traits. We find some interesting differences between the two models, primarily that in the two-locus sexual selection model shifts between preference and trait regimes occur more often with both weak and strong preferences, compared to intermediate preference strengths. We discuss the implications of our results for the evolution of pheromone blends and male responses during speciation in moths, a case that seems to match the assumptions of our model.


Genetic drift Moth Population genetic model Sexual selection Speciation Stochasticity 



The authors thank J. Adamson, A. Frame, S. Dhole, J. McKinnon, and two anonymous reviewers for comments on the manuscript and N. Barton, R. Servedio and especially T. Paixão for discussion. We also thank A. Faucci, M.P. Miglietta and F. Santini for the invitation to contribute to this edition. MRS and JTR were funded by NSF DEB 0919018 EB was funded by the NSF REU supplement DEB-1026740.


  1. Alatalo, R. V., Carlson, A., & Lundberg, A. (1988). The costs of mate choice in the pied flycatcher. Animal Behaviour, 36, 289–291.CrossRefGoogle Scholar
  2. Barton, N. H., & Turelli, M. (1991). Natural and sexual selection on many loci. Genetics, 127, 229–255.PubMedGoogle Scholar
  3. Bengtsson, B. O., & Lofstedt, C. (2007). Direct and indirect selection in moth pheromone evolution: Population genetical simulations of asymmetric sexual interactions. Biological Journal of the Linnean Society, 90, 117–123.CrossRefGoogle Scholar
  4. Butlin, R. K., & Trickett, A. J. (1997). Can population genetic simulations help to interpret pheromone evolution? In R. T. Carde & A. K. Minks (Eds.), Insect pheromone research: New directions (pp. 548–562). New York: Chapman and Hall.CrossRefGoogle Scholar
  5. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA, USA: Sinauer Associates.Google Scholar
  6. De Jong, M. C. M., & Sabelis, M. W. (1991). Limits to runaway sexual selection: The wallflower paradox. Journal of Evolutionary Biology, 4, 637–655.CrossRefGoogle Scholar
  7. Foster, S. P., & Ayers, R. H. (1996). Multiple mating and its effects in the lightbrown apple moth, Epiphyas postvittana (Walker). Journal of Insect Physiology, 42, 657–667.CrossRefGoogle Scholar
  8. Gascoigne, J., Berec, L., Gregory, S., & Courchamp, F. (2009). Dangerously few liasons: A review of mate-finding allee effects. Population Ecology, 51, 355–372.CrossRefGoogle Scholar
  9. Gomulkiewicz, R. S., & Hastings, A. (1990). Ploidy and evolution by sexual selection: A comparison of haploid and diploid female choice models near fixation equilibria. Evolution, 44, 757–770.CrossRefGoogle Scholar
  10. Gotthard, K., Nylin, S., & Wiklund, C. (1999). Mating system evolution in response to search costs in the speckled wood butterfly, Pararge aegeria. Behavioral Ecology and Sociobiology, 45, 424–429.CrossRefGoogle Scholar
  11. Gould, F., Estock, M., Hillier, N. K., Powell, B., Groot, A. T., Ward, C. M., et al. (2010). Sexual isolation of male moths explained by a single pheromone response QTL containing four odorant receptor genes. Proceedings of the National Academy of Sciences USA, 107, 8660–8665.CrossRefGoogle Scholar
  12. Gould, F., Groot, A. T., Vasquez, G. M., & Schal, C. (2009). Sexual communication in Lepidoptera: A need for wedding genetics, biochemistry, and molecular biology, chapter 10. In M. Frantisek & M. R. Goldsmith (Eds.) Molecular biology and genetics of the Lepidoptera. London: Taylor and Francis Group.Google Scholar
  13. Greenspoon, P. B., & Otto, S. P. (2009). Evolution by Fisherian sexual selection in diploids. Evolution, 63, 1076–1083.PubMedCrossRefGoogle Scholar
  14. Groot, A. T., Santangelo, R. G., Ricci, E., Brownie, C., Gould, F., & Schal, C. (2007). Differential attraction of Heliothis subflexa males to synthetic pheromone lures in eastern US and western Mexico. Journal of Chemical Ecology, 33, 353–368.PubMedCrossRefGoogle Scholar
  15. Hedrick, A. V., & Dill, L. M. (1993). Mate choice by female crickets is influenced by predation risk. Animal Behaviour, 46, 193–196.CrossRefGoogle Scholar
  16. Heisler, I. L., & Curtsinger, J. W. (1990). Dynamics of sexual selection in diploid populations. Evolution, 44, 1164–1176.CrossRefGoogle Scholar
  17. Innan, H., & Stephan, W. (2001). Selection intensity against deleterious mutations in RNA secondary structures and rate of compensatory nucleotide substitutions. Genetics, 159, 380–399.Google Scholar
  18. Kimura, M. (1954). Process leading to quasi-fixation of genes in natural populations due to random fluctuation of selection intensities. Genetics, 39, 280–295.PubMedGoogle Scholar
  19. Kirkpatrick, M. (1982). Sexual selection and the evolution of female choice. Evolution, 36, 1–12.CrossRefGoogle Scholar
  20. Kirkpatrick, M., & Nuismer, S. L. (2004). Sexual selection can constrain sympatric speciation. Proceedings of the Royal Society of London B, Biological Sciences, 271, 687–693.CrossRefGoogle Scholar
  21. Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Science, USA, 78, 3721–3725.CrossRefGoogle Scholar
  22. Lenormand, T., Roze, D., & Roussett, F. (2009). Stochasticity in evolution. Trends in Ecology & Evolution, 24, 157–165.CrossRefGoogle Scholar
  23. Linn, C. E., Young, M. S., Gendle, M., Glover, T. J., & Roelofs, W. L. (1997). Sex pheromone blend discrimination in two races and hybrids of the European core borer moth, Ostrinia nubilalis. Physiological Entomology, 22, 212–223.CrossRefGoogle Scholar
  24. Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.Google Scholar
  25. McNeil, J. N. (1991). Behavioral ecology of pheromone-mediated communication in moths and its importance in the use of pheromone traps. Annual Review of Entomology, 36, 407–430.CrossRefGoogle Scholar
  26. Michalakis, Y., & Slatkin, M. (1996). Interaction of selection and recombination in the fixation of negative-epistatic genes. Genetical Research, 67, 257–269.PubMedCrossRefGoogle Scholar
  27. Otto, S. P., Servedio, M. R., & Nuismer, S. L. (2008). Frequency-dependent selection and the evolution of assortative mating. Genetics, 179, 2091–2112.PubMedCrossRefGoogle Scholar
  28. Page, K. M., & Nowak, M. A. (2002). Unifying evolutionary dynamics. Journal of Theoretical Biology, 219, 93–98.PubMedGoogle Scholar
  29. Panhuis, T. M., Butlin, R., Zuk, M., & Tregenza, T. (2001). Sexual selection and speciation. Trends in Ecology & Evolution, 16, 364–371.CrossRefGoogle Scholar
  30. Phelan, P. L. (1992). Evolution of sex pheromones and the role of asymmetric tracking. In B. D. Roitberg, & M. B. Isman (Eds.) Insect chemical ecology: an evolutionary approach, (pp. 265–314).Google Scholar
  31. Phillips, P. C. (1996). Waiting for a compensatory mutation: Phase zero of the shifting-balance process. Genetical Reserach, 67, 271–283.CrossRefGoogle Scholar
  32. Proshold, F. I. (1996). Reproductive capacity of laboratory-reared gypsy moths (Lepidoptera: Lymantriidae): Effect of age of female at time of mating. Journal of Economic Entomology, 89, 337–342.Google Scholar
  33. Ritchie, M. G. (2007). Sexual selection and speciation. Annual Review of Ecology Evolution and Systematics, 38, 79–102.CrossRefGoogle Scholar
  34. Roelofs, W. L., & Rooney, A. P. (2003). Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proceedings of the National Academy of Sciences, USA, 100, 9179–9184.CrossRefGoogle Scholar
  35. Rutledge, R. A. (1970). The survival of epistatic gene complexes in subdivided populations. Unpublished PhD thesis, Columbia University.Google Scholar
  36. Servedio, M. R. (2011). Limits to the evolution of assortative mating by female choice under restricted gene flow. Proceedings of the Royal Society of London, B, Biological Sciences, 278, 179–187.CrossRefGoogle Scholar
  37. Svensson, M. G. E., Marling, E., & Lofqvist, J. (1998). Mating behavior and reproductive potential in the turnip moth Agrotis segetum (Lepidoptera: Noctuidae). Journal of Insect Behavior, 11, 343–359.CrossRefGoogle Scholar
  38. Unnithan, G. C., & Paye, S. O. (1991). Mating, longevity, fecundity, and egg fertility of Chilo partellus (Lepidoptera: Pyralidae): effects of delayed or successive matings and their relevance to pheromonal control methods. Environmental Entomology, 20, 150–155.Google Scholar
  39. Uyeda, J. C., Arnold, S. J., Hohenlohe, P. A., & Mead, L. S. (2009). Drift promotes speciation by sexual selection. Evolution, 63, 583–594.PubMedCrossRefGoogle Scholar
  40. Vickers, R. A. (1997). Effect of delayed mating on oviposition pattern, fecundity and fertility in codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Australian Journal of Entomology, 36, 179–182.CrossRefGoogle Scholar
  41. Wright, S. (1931). Evolution in mendelian populations. Genetics, 16, 97–159.PubMedGoogle Scholar
  42. Wu, C.-I. (1985). A stochastic simulation study on speciation by sexual selection. Evolution, 39, 66–82.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Elizabeth L. Bergen
    • 1
  • Jonathan T. Rowell
    • 1
  • Fred Gould
    • 2
  • Maria R. Servedio
    • 1
    Email author
  1. 1.Department of BiologyUniversity of North CarolinaChapel HillUSA
  2. 2.Department of EntomologyNorth Carolina State UniversityRaleighUSA

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