Behavioral Ecology and Sociobiology

, Volume 66, Issue 10, pp 1429–1436 | Cite as

Reinforcement of male mate preferences in sympatric killifish species Lucania goodei and Lucania parva

  • Olivia Gregorio
  • Emma L. Berdan
  • Genevieve M. Kozak
  • Rebecca C. Fuller
Original Paper

Abstract

Reinforcement occurs when reduced hybrid fitness leads to the evolution of a stronger prezygotic isolation. Populations sympatric with closely related species, where hybridization occurs, are predicted to have stronger mate preferences than allopatric populations. The reinforcement of male mate preference is thought to be rarer than the reinforcement of female preference, but this inference may be biased by the lack of studies on male preference. We tested male mate preferences from sympatric and allopatric populations of two closely related species of killifish: Lucania goodei and Lucania parva. We found that sympatric males had greater preferences for conspecific females than allopatric males. Furthermore, conspecific preferences in allopatric populations were weakest when these populations were geographically distant (>50 km) from those of heterospecifics. Our data suggest that reinforcement has contributed to male conspecific preference and speciation in Lucania.

Keywords

Reinforcement Speciation Male mate preference Prezygotic isolation Hybridization 

Notes

Acknowledgments

This work was funded by a National Science Foundation Grant (DEB 0953716) to R. C. Fuller and a Doctoral Dissertation Improvement Grant (DEB 1110658) to E. L. Berdan and R. C. Fuller. C. Baldeck and A. Johnson assisted with fish collection. Four anonymous reviewers and J. Lindström provided constructive comments on the manuscript.

Ethical standards

All experiments comply with the current laws of the United States and were approved by the University of Illinois Institutional Animal Care and Use Committee (Protocol numbers 08183 and 09306).

Conflicts of interest

The authors declare that they have no conflicts of interest.

References

  1. Albert AYK, Schluter D (2004) Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection? Evolution 58:1099–1107PubMedGoogle Scholar
  2. Arndt RGE (1971) Ecology and behavior of the cyprinodont fishes Adinia xenica, Lucania parva, Lucania goodei, and Leptolucania ommata. Dissertation, Cornell UniversityGoogle Scholar
  3. Berdan EB, Fuller RC (2012) A test for environmental effects on behavioral isolation in two species of killifish. Evolution. doi: 10.1111/j.1558-5646.2011.01646.x
  4. Bierbach D, Girndt A, Hamfler S, Klein M, Mucksch F, Penshorn M, Schwinn M, Zimmer C, Schlupp I, Streit B, Plath M (2011) Male fish use prior knowledge about rivals to adjust their mate choice. Biol Lett 7:349–351PubMedCrossRefGoogle Scholar
  5. Booksmythe I, Jennions MD, Backwell PRY (2011) Male fiddler crabs prefer conspecific females during simultaneous, but not sequential, mate choice. Anim Behav 81:775–778CrossRefGoogle Scholar
  6. Butlin RK (1987a) Speciation by reinforcement. Trends Ecol Evol 2:8–13PubMedCrossRefGoogle Scholar
  7. Butlin RK (1987b) Species, speciation, and reinforcement. Am Nat 130:461–464CrossRefGoogle Scholar
  8. Butlin RK (1989) Reinforcement of premating isolation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, pp 158–179Google Scholar
  9. Butlin RK, Ritchie MG (1994) Mating behaviour and speciation. In: Slater PJB, Halliday TR (eds) Behaviour and evolution. Cambridge University Press, Cambridge, pp 43–79Google Scholar
  10. Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381CrossRefGoogle Scholar
  11. Dobzhansky TG (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  12. Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654PubMedCrossRefGoogle Scholar
  13. Espinedo CM, Gabor CR, Aspbury AS (2010) Males, but not females, contribute to sexual isolation between two sympatric species of Gambusia. Evol Ecol 24:865–878CrossRefGoogle Scholar
  14. Foster NR (1967) Comparative studies on the biology of killifishes. Dissertation, Cornell UniversityGoogle Scholar
  15. Fuller RC (2001) Patterns in male breeding behaviors in the bluefin killifish, Lucania goodei: A field study (Cyprinodontiformes: Fundulidae). Copeia 2001:823–828CrossRefGoogle Scholar
  16. Fuller RC (2008) Genetic incompatibilities in killifish and the role of environment. Evolution 62:3056–3068PubMedCrossRefGoogle Scholar
  17. Fuller RC, Noa LA (2008) Distribution and stability of sympatric populations of Lucania goodei and L. parva across Florida. Copeia 2008:699–707CrossRefGoogle Scholar
  18. Fuller RC, Travis J (2001) A test for male parental care in a fundulid, the bluefin killifish, Lucania goodei. Environ Biol Fish 61:419–426CrossRefGoogle Scholar
  19. Fuller RC, McGhee KE, Schrader M (2007) Speciation in killifish and the role of salt tolerance. J Evol Biol 20:1962–1975PubMedCrossRefGoogle Scholar
  20. Gabor CR, Ryan MJ (2001) Geographical variation in reproductive character displacement in mate choice by male sailfin mollies. Proc R Soc Lond B 268:1063–1070CrossRefGoogle Scholar
  21. Gabor CR, Ryan MJ, Morizot DC (2005) Character displacement in sailfin mollies, Poecilia latipinna: allozymes and behavior. Environ Biol Fish 73:75–88CrossRefGoogle Scholar
  22. Goldberg EE, Lande R (2006) Ecological and reproductive character displacement on an environmental gradient. Evolution 60:1344–1357PubMedGoogle Scholar
  23. Houde AE (1997) Sex, color, and mate choice in guppies. Monographs in behavior and ecology. Princeton University Press, PrincetonGoogle Scholar
  24. Howard DJ (1993) Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 46–69Google Scholar
  25. Hubbs C, Walker B, Johnson R (1943) Hybridization in nature between species of American cyprinodont fishes. Contrib Lab Vertebr Biol Univ Mich 23:1–21Google Scholar
  26. Kirkpatrick M (2001) Reinforcement during ecological speciation. Proc R Soc Lond B 268:1259–1263CrossRefGoogle Scholar
  27. Kirkpatrick M, Servedio MR (1999) The reinforcement of mating preferences on an island. Genetics 151:865–884PubMedGoogle Scholar
  28. Kozak GM, Reisland M, Boughman JW (2009) Sex differences in mate recognition and conspecific preference in species with mutual mate choice. Evolution 63:353–365PubMedCrossRefGoogle Scholar
  29. Kozak GM, Rudolph AB, Colon BL, Fuller RC (2012) Postzygotic isolation evolves before prezygotic isolation between fresh and saltwater populations of the rainwater killifish, Lucania parva. Int J Evol Biol 2012. doi: 10.1155/2012/523967
  30. Kronforst MR, Young LG, Gilbert LE (2007) Reinforcement of mate preference among hybridizing Heliconius butterflies. J Evol Biol 20:278–285PubMedCrossRefGoogle Scholar
  31. Lee DS, Gilbert CR, Hocutt CH, Jenkins RE, McAllister DE, Stauffer JR Jr (1980) Atlas of North American fishes. North Carolina State Museum, RaleighGoogle Scholar
  32. Lemmon AR, Smadja C, Kirkpatrick M (2004) Reproductive character displacement is not the only possible outcome of reinforcement. J Evol Biol 17:177–183PubMedCrossRefGoogle Scholar
  33. Magurran AE, Ramnarine IW (2005) Evolution of mate discrimination in a fish. Curr Biol 15:R867–R868PubMedCrossRefGoogle Scholar
  34. Makowicz AM, Plath M, Schlupp I (2010) Male guppies (Poecilia reticulata) adjust their mate choice behaviour to the presence of an audience. Behaviour 147:1657–1674CrossRefGoogle Scholar
  35. McGhee KE, Travis J (2010) Repeatable behavioural type and stable dominance rank in the bluefin killifish. Anim Behav 79:497–507CrossRefGoogle Scholar
  36. Noor MAF (1995) Speciation driven by natural-selection in Drosophila. Nature 375:674–675PubMedCrossRefGoogle Scholar
  37. Noor MAF (1999) Reinforcement and other consequences of sympatry. Heredity 83:503–508PubMedCrossRefGoogle Scholar
  38. O'Rourke CF, Mendelson TC (2010) Male and female preference for conspecifics in a fish with male parental care (Percidae: Catonotus). Behav Process 85:157–162CrossRefGoogle Scholar
  39. Ortiz-Barrientos D, Grealy A, Nosil P (2009) The genetics and ecology of reinforcement; implications for the evolution of prezygotic isolation in sympatry and beyond. Ann N Y Acad Sci 1168:156–182PubMedCrossRefGoogle Scholar
  40. Peterson MA, Honchak BM, Locke SE, Beeman TE, Mendoza J, Green J, Buckingham KJ, White MA, Monsen KJ (2005) Relative abundance and the species-specific reinforcement of male mating preference in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone. Evolution 59:2639–2655PubMedGoogle Scholar
  41. Ramsey J, Bradshaw HD, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534PubMedGoogle Scholar
  42. Ratcliffe LG, Grant PR (1983) Species recognition in Darwin's finches (Geospiza, Gould). II. Geographic-variation in mate preference. Anim Behav 31:1154–1165CrossRefGoogle Scholar
  43. Saetre GP, Moum T, Bures S, Kral M, Adamjan M, Moreno J (1997) A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387:589–592CrossRefGoogle Scholar
  44. Servedio MR (2007) Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement. Evolution 61:2772–2789PubMedCrossRefGoogle Scholar
  45. Servedio MR, Lande R (2006) Population genetic models of male and mutual mate choice. Evolution 60:674–685PubMedGoogle Scholar
  46. Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34:339–364CrossRefGoogle Scholar
  47. Svensson EI, Karlsson K, Friberg M, Eroukhmanoff F (2007) Gender differences in species recognition and the evolution of asymmetric sexual isolation. Curr Biol 17:1943–1947PubMedCrossRefGoogle Scholar
  48. Swenton DM (2011) Sex differences in mate preference between two hybridizing species of poeciliid fish. Ethology 117:208–216CrossRefGoogle Scholar
  49. Tobler M, Schlupp I, Plath M (2008) Does divergence in female mate choice affect male size distributions in two cave fish populations? Biol Lett 4:452–454PubMedCrossRefGoogle Scholar
  50. Waage JK (1979) Reproductive character displacement in Calopteryx (Odonata, Calopterygidae). Evolution 33:104–116CrossRefGoogle Scholar
  51. Yukilevich R (2012) Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution 66:1430–1446PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Olivia Gregorio
    • 1
  • Emma L. Berdan
    • 1
  • Genevieve M. Kozak
    • 1
  • Rebecca C. Fuller
    • 1
  1. 1.Department of Animal BiologyUniversity of IllinoisChampaignUSA

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