Naturwissenschaften

, Volume 97, Issue 8, pp 769–774

Complementary effect of natural and sexual selection against immigrants maintains differentiation between locally adapted fish

  • Martin Plath
  • Rüdiger Riesch
  • Alexandra Oranth
  • Justina Dzienko
  • Nora Karau
  • Angela Schießl
  • Stefan Stadler
  • Adriana Wigh
  • Claudia Zimmer
  • Lenin Arias-Rodriguez
  • Ingo Schlupp
  • Michael Tobler
Short Communication

Abstract

Adaptation to ecologically heterogeneous environments can drive speciation. But what mechanisms maintain reproductive isolation among locally adapted populations? Using poeciliid fishes in a system with naturally occurring toxic hydrogen sulfide, we show that (a) fish from non-sulfidic sites (Poecilia mexicana) show high mortality (95 %) after 24 h when exposed to the toxicant, while locally adapted fish from sulfidic sites (Poecilia sulphuraria) experience low mortality (13 %) when transferred to non-sulfidic water. (b) Mate choice tests revealed that P. mexicana females exhibit a preference for conspecific males in non-sulfidic water, but not in sulfidic water, whereas P. sulphuraria females never showed a preference. Increased costs of mate choice in sulfidic, hypoxic water, and the lack of selection for reinforcement due to the low survival of P. mexicana may explain the absence of a preference in P. sulphuraria females. Taken together, our study may be the first to demonstrate independent—but complementary—effects of natural and sexual selection against immigrants maintaining differentiation between locally adapted fish populations.

Keywords

Ecological speciation Female choice Hydrogen sulfide Isolation-by-adaptation Reciprocal translocation experiment Reproductive isolation 

Supplementary material

114_2010_691_MOESM1_ESM.doc (1.9 mb)
ESM 1(DOC 1.89 MB)

References

  1. Alvarez del Villar J (1948) Descripción de una nueva especie de Mollienisia capturada en Baños del Azufre, Tabasco (Pisces, Poeciliidae). Anal Esc Nac Cien Biol 5:275–281Google Scholar
  2. Dettman J, Sirjusingh C, Kohn L, Anderson J (2007) Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447:585–588CrossRefPubMedGoogle Scholar
  3. Hendry AP (2004) Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. Evol Ecol Res 6:1219–1236Google Scholar
  4. Langerhans RB, Gifford M, Joseph E (2007) Ecological speciation in Gambusia fishes. Evolution 61:2056–2074CrossRefPubMedGoogle Scholar
  5. Lorch PD, Proloux S, Rowe L, Day T (2003) Condition dependent sexual selection accelerates adaptation by natural selection. Evol Ecol Res 5:867–881Google Scholar
  6. Magurran AE, Ramnarine IW (2005) Evolution of mate discrimination in a fish. Curr Biol 15:R867–R868CrossRefPubMedGoogle Scholar
  7. Matute DR, Novak CJ, Coyne J (2009) Temperature-based extrinsic reproductive isolation in two species of Drosophila. Evolution 63:595–612CrossRefPubMedGoogle Scholar
  8. Nosil P, Crespi B, Sandoval C (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:440–443CrossRefPubMedGoogle Scholar
  9. Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  10. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402CrossRefPubMedGoogle Scholar
  11. Parzefall J (1969) Zur vergleichenden Ethologie verschiedener Mollienesia-Arten einschließlich einer Höhlenform von M. sphenops. Behaviour 33:1–37CrossRefPubMedGoogle Scholar
  12. Peters N, Peters G, Parzefall J, Wilkens H (1973) Über degenerative und konstruktive Merkmale bei einer phylogenetisch jungen Höhlenform von Poecilia sphenops (Pisces, Poeciliidae). Int Rev Ges Hydrobiol 58:417–436CrossRefGoogle Scholar
  13. Plath M (2008) Male mating behavior and costs of sexual harassment for females in cavernicolous and extremophile populations of Atlantic mollies (Poecilia mexicana). Behaviour 145:73–98CrossRefGoogle Scholar
  14. Plath M, Tobler M (2010) Subterranean fishes of Mexico (Poecilia mexicana, Poeciliidae). In: Trajano E, Bichuette ME, Kapoor BG (eds) Biology of subterranean fishes. Science Publishers, Enfield, pp 281–330Google Scholar
  15. Plath M, Tobler M, Riesch R, García de León FJ, Giere O, Schlupp I (2007) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwiss 94:991–996CrossRefPubMedGoogle Scholar
  16. Plath M, Hermann B, Schröder C, Riesch R, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2010) Catastrophic flood does not lead to loss of small-scale genetic differentiation among locally adapted fish populations. BMC Evol Biol (in press)Google Scholar
  17. Riesch R, Schlupp I, Plath M (2008) Female sperm-limitation in natural populations of a sexual/asexual mating complex (Poecilia latipinna, P. formosa). Biol Lett 4:266–269CrossRefPubMedGoogle Scholar
  18. Riesch R, Plath M, García de León FJ, Schlupp I (2010a) Convergent life-history shifts: toxic environments result in big babies in two clades of poeciliids. Naturwiss 97:133–141CrossRefPubMedGoogle Scholar
  19. Riesch R, Plath M, Schlupp I (2010b) Toxic hydrogen sulfide and dark caves: life history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology 91:1494–1505CrossRefPubMedGoogle Scholar
  20. Rundle HD, Schluter D (1998) Reinforcement of stickleback mate preferences: sympatry breeds contempt. Evolution 52:200–208CrossRefGoogle Scholar
  21. Rundle HD, Nagel L, Boughman J, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–308CrossRefPubMedGoogle Scholar
  22. Schlupp I, Riesch R, Tobler M, Plath M, Parzefall J, Schartl M (2010) A novel sexually selected trait in poeciliid fishes: Female preference for mustache-like, rostral filaments in male Poecilia sphenops. Behav Ecol Sociobiol (in press)Google Scholar
  23. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380CrossRefPubMedGoogle Scholar
  24. Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528CrossRefGoogle Scholar
  25. Tobler M (2009) Does a predatory insect contribute to the divergence between cave- and surface-adapted fish populations? Biol Lett 5:506–509CrossRefPubMedGoogle Scholar
  26. Tobler M, Plath M (2009) Threatened fishes of the world: Poecilia sulphuraria (Alvarez, 1948) (Poeciliidae). Environ Biol Fish 85:333–334CrossRefGoogle Scholar
  27. Tobler M, Plath M (2010) Living in extreme environments. In: Evans J, Pilastro A, Schlupp I (eds) Ecology and evolution of livebearing fishes (Poeciliidae). Chicago University Press, Chicago (in press)Google Scholar
  28. Tobler M, Schlupp I, Riesch R, García de León FJ, Plath M (2008a) Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulfidic habitat. J Fish Biol 72:1–11CrossRefGoogle Scholar
  29. Tobler M, DeWitt TJ, Schlupp I, Garcia de Leon FJ, Herrmann R, Feulner P, Tiedemann R, Plath M (2008b) Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 62:2643–2649CrossRefPubMedGoogle Scholar
  30. Tobler M, Riesch R, Tobler CM, Schulz-Mirbach T, Plath M (2009a) Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations. J Evol Biol 22:2298–2304CrossRefPubMedGoogle Scholar
  31. Tobler M, Riesch R, Tobler CM, Plath M (2009b) Compensatory behavior in response to sulfide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol Ecol Res 11:935–948Google Scholar
  32. Walling CA, Royle NJ, Lindström J, Metcalfe NB (2010) Do female association preferences predict the likelihood of reproduction? Behav Ecol Sociobiol 64:541–548CrossRefGoogle Scholar
  33. Winemiller KO (1989) Development of dermal lip protuberances for aquatic surface respiration in South American characid fishes. Copeia 1989:382–390CrossRefGoogle Scholar
  34. Wong BBM, Jennions MD (2003) Costs influence male mate choice in a freshwater fish. Proc R Soc Lond B Biol Sci 270:S36–S38CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Martin Plath
    • 1
  • Rüdiger Riesch
    • 2
  • Alexandra Oranth
    • 1
  • Justina Dzienko
    • 1
  • Nora Karau
    • 1
  • Angela Schießl
    • 1
  • Stefan Stadler
    • 1
  • Adriana Wigh
    • 1
  • Claudia Zimmer
    • 1
  • Lenin Arias-Rodriguez
    • 3
  • Ingo Schlupp
    • 2
  • Michael Tobler
    • 4
  1. 1.Department of Ecology and EvolutionJ.W. Goethe University of FrankfurtFrankfurt am MainGermany
  2. 2.Department of ZoologyUniversity of OklahomaNormanUSA
  3. 3.División Académica de Ciencias BiológicasUniversidad Juárez Autónoma de Tabasco (UJAT)VillahermosaMéxico
  4. 4.Department of Biology and Department of Wildlife and Fisheries SciencesTexas A&M UniversityCollege StationUSA

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