Skip to main content
SpringerLink
Log in

Quantification of Reproductive Isolating Barriers Between Two Naturally Hybridizing Killifish Species

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Understanding the relative importance of various reproductive barriers to the early stages of speciation is an essential question in evolutionary biology. The closely related killifishes Fundulus heteroclitus and F. grandis occasionally hybridize in a small region in coastal Northeastern Florida showing that while barriers to reproduction exist, they are incomplete. The objective of this study was to elucidate barriers to reproduction between F. heteroclitus and F. grandis in the lab, as well as to quantify their strengths and relative contributions to reproductive isolation. Pre-zygotic (mating and fertilization) and post-zygotic (hatching) barriers were investigated by performing a variety of choice and no-choice laboratory mating experiments. Under no-choice conditions, barriers to mating had the greatest influence on hybrid production in F. grandis, whereas hatching barriers contributed to the majority of reproductive isolation in F. heteroclitus. Under choice conditions, however, pre-zygotic barriers had the greatest influence on hybrid production in both species. The total reproductive isolation that was observed in females of each species was stronger in F. heteroclitus than in F. grandis, and was nearly complete in F. heteroclitus females under choice conditions and was of moderate strength in F. grandis females. These results reveal an asymmetry in the potential gene flow between these two species, with F. grandis being more likely to hybridize than F. heteroclitus in the absence of environmental influences. No-choice backcrosses were also conducted and showed that at least some F1 hybrids are fertile. The observation that pre-zygotic barriers tend to be stronger than post-zygotic barriers in the early stages of speciation is consistent with similar studies in other organisms.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Able, K., & Hagan, S. (2003). Impact of common reed, Phragmites australis, on essential fish habitat: Influence on reproduction, embryological development, and larval abundance of Mummichog (Fundulus heteroclitus). Estuaries, 26, 40–50.

    Article  Google Scholar 

  • Able, K., & Hata, D. (1984). Reproductive behavior in the Fundulus heteroclitus-F. grandis complex. Copeia, 1984, 820–825.

    Article  Google Scholar 

  • Berdan, E. L., & Fuller, R. C. (2012). A test for environmental effects on behavioral isolation in two species of killifish. Evolution, 66, 3224–3237.

    Article  Google Scholar 

  • Bernardi, G., & Powers, D. A. (1995). Phylogenetic relationships among nine species from the genus Fundulus (Cyprinodontiformes, Fundulidae) inferred from sequences of the cytochrome B gene. Copeia, 1995, 469–473.

    Article  Google Scholar 

  • Case, T., & Taper, M. (2000). Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders. The American Naturalist, 155, 583–605.

    Article  CAS  Google Scholar 

  • Coyne, J. A., & Orr, A. H. (2004). Speciation. Sunderland: Sinauer Associates, Inc.

    Google Scholar 

  • Coyne, J. A., & Orr, H. A. (1989). Patterns of speciation in Drosophila. Evolution, 43, 362–381.

    Article  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (1998). The evolutionary genetics of speciation. Philosophical Transactions of the Royal Society of London B, 353, 287–305.

    Article  CAS  Google Scholar 

  • Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.

    Google Scholar 

  • Dobzhansky, T. (1940). Speciation as a stage in evolutionary divergence. The American Naturalist, 74, 312–321.

    Article  Google Scholar 

  • Ellis, W., & Bell, S. (2004). Conditional use of mangrove habitats by fishes: Depth as a due to avoid predators. Estuaries, 27, 966–976.

    Article  Google Scholar 

  • Elmer, K. R., Lehtonen, T. K., & Meyer, A. (2009). Color assortative mating contributes to sympatric divergence of neotropical cichlid fish. Evolution, 63, 2750–2757.

    Article  Google Scholar 

  • Foster, N. R. (1967). Trends in the evolution of reproductive behavior in killifishes. In: F. M. Bayer et al., (Eds.), Proceedings of the international conference on tropical oceanography (pp. 549–566). Miami, FL: University of Miami Institute of Marine Sciences.

    Google Scholar 

  • Fricke, C., & Arnqvist, G. (2004). Conspecific sperm precedence in flour beetles. Animal Behaviour, 67, 729–732.

    Article  Google Scholar 

  • Galleher, S. N., Gilg, M. R., & Smith, K. J. (2010). Comparison of larval thermal maxima between Fundulus heteroclitus and F. grandis. Fish Physiology and Biochemistry, 36, 731–740.

    Article  CAS  Google Scholar 

  • Galleher, S. N., Gonzalez, I., Gilg, M. R., & Smith, K. J. (2009). Larvae and juvenile Fundulus heteroclitus abundance and distribution in Northeast Florida salt marshes. Southeastern Naturalist, 8, 495–502.

    Article  Google Scholar 

  • Geyer, L. B., & Palumbi, S. R. (2005). Conspecific sperm precedence in two species of tropical sea urchins. Evolution, 59, 97–105.

    Article  Google Scholar 

  • Gonzalez, I., Levin, M., Jermanus, S., Watson, B., & Gilg, M. R. (2009). Genetic assessment of species ranges in Fundulus heteroclitus and F. grandis in northeastern Florida salt marshes. Southeastern Naturalist, 8, 227–243.

    Article  Google Scholar 

  • Grady, J. M., Coykendall, D. K., Collette, B. B., & Quattro, J. M. (2001). Taxonomic diversity, origin, and conservation status of Bermuda killifishes (Fundulus) based on mitochondrial cytochrome b phylogenies. Conservation Genetics, 2, 41–52.

    Article  CAS  Google Scholar 

  • Gregorio, O., Berdan, E. L., Kozak, G. M., & Fuller, R. C. (2012). Reinforcement of male mate preference in sympatric killifish species Lucania goodie and Lucania parva. Behavioral Ecology and Sociobiology, 66, 1429–1436.

    Article  Google Scholar 

  • Hipperson, H., Dunning, L. T., Baker, W. J., Butlin, R. K., Hutton, I., Papadopulos, A. S. T., et al. (2016). Ecological speciation in sympatric palms: 2. Pre- and post-zygotic isolation. Journal of Evolutionary Biology, 29, 2143–2156.

    Article  CAS  Google Scholar 

  • Howard, D., Gregory, P., Chu, J., & Cain, M. (1998). Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution, 52, 511–516.

    Article  Google Scholar 

  • Howard, D. J. (1993). Reinforcement: Origin, dynamics and fate of an evolutionary hypothesis. In R. G. Harrison (Ed.), Hybrid zones and the evolutionary process (pp. 46–69). New York: Oxford University Press.

    Google Scholar 

  • Hsiao, S., & Meier, A. (1989). Comparison of semilunar cycles of spawning activity in Fundulus grandis and F. heteroclitus held under constant laboratory conditions. Journal of Experimental Zoology, 252, 213–218.

    Article  Google Scholar 

  • Hsiao, S. M., Limesand, S. W., & Wallace, R. A. (1996). Semilunar follicular cycle of an intertidal fish: The Fundulus model. Biology of Reproduction, 54, 809–818.

    Article  CAS  Google Scholar 

  • Hsiao, S. -M., & Meier, A. H. (1986). Spawning cycles of the Gulf killifish, Fundulus grandis, in closed circulation systems. Journal of Experimental Zoology, 240, 105–112.

    Article  Google Scholar 

  • Jordan, D., & Evermann, B. (1898). The fishes of North and Middle America: A descriptive catalogue of the species of fish-like vertebrates found in the waters of North America, north of the Isthmus of Panama, 47th ed. US Government Printing Office, Washington, District of Columbia.

  • Kneib, R. (1986). The role of Fundulus heteroclitus in salt marsh trophic dynamics. American Zoologist, 26, 259–269.

    Article  Google Scholar 

  • Kneib, R. T. (1984). Patterns in the utilization of the intertidal salt marsh by larvae and juveniles of Fundulus heteroclitus (Linnaeus) and Fundulus luciae (Baird). Journal of Experimental Marine Biology and Ecology, 83, 41–51.

    Article  Google Scholar 

  • Lackey, A. C. R., & Boughman, J. W. (2017). Evolution of reproductive isolation in stickleback fish. Evolution, 71, 357–372.

    Article  Google Scholar 

  • Laurie, C. C. (1997). The weaker sex is heterogametic: 75 years of Haldane’s rule. Genetics, 147, 937–951.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lowry, D. B., Modliszewski, J. L., Wright, K. M., Wu, C. A., & Willis, J. H. (2008). The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosophical Transactions of the Royal Society of London B, 363, 3009–3021.

    Article  Google Scholar 

  • Ludlow, A. M., & Magurran, A. E. (2006). Gametic isolation in guppies (Poecilia reticulata). Proceedings of the Royal Society of London B, 273, 2477–2482.

    Article  CAS  Google Scholar 

  • Martin, M. D., & Mendelson, T. C. (2016). The accumulation of reproductive isolation in early stages of divergence supports a role for sexual selection. Journal of Evolutionary Biology, 29, 676–689.

    Article  CAS  Google Scholar 

  • Martin, M. D., & Mendelson, T. C. (2018). Hybrid sterility increases with genetic distance in snubnose darters (Percidae: Etheostoma). Environmental Biology of Fishes, 101, 215–221.

    Article  Google Scholar 

  • Martin, N. H., & Willis, J. H. (2007). Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution, 61, 68–82.

    Article  Google Scholar 

  • Martin, N. H., & Willis, J. H. (2010). Geographical variation in postzygotic isolation and its genetic basis within and between two Mimulus species. Philosophical Transactions of the Royal Society of London B, 365, 2469–2478.

    Article  Google Scholar 

  • Martín-Coello, J., Benavent-Corai, J., Roldan, E. R. S., & Gomendio, M. (2009). Sperm competition promotes asymmetries in reproductive barriers between closely related species. Evolution, 63, 613–623.

    Article  Google Scholar 

  • Matsubayashi, K. W., & Katakura, H. (2009). Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution, 63, 2563–2580.

    Article  Google Scholar 

  • Mayr, E. (1940). Speciation phenomena in birds. The American Naturalist, 74, 249–278.

    Article  Google Scholar 

  • Mayr, E. (1942). Systematics and the origin of species, from the viewpoint of a zoologist. Cambridge: Harvard University Press.

    Google Scholar 

  • Mayr, E. (2000). The biological species concept. In Q. D. Wheeler & R. Meier (Eds.), Species concepts and phylogenetic theory: A debate (pp. 17–29). New York: Columbia University Press.

    Google Scholar 

  • Mendelson, T. C. (2003). Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma). Evolution, 57, 317–327.

    Article  Google Scholar 

  • Mendelson, T. C., Imhoff, V. E., & Venditti, J. J. (2007). The accumulation of reproductive barriers during speciation: Postmating barriers in two behaviorally isolated species of darters (Percidae: Etheostoma). Evolution, 61, 2596–2606.

    Article  Google Scholar 

  • Muller, H. J. (1939). Reversibility in evolution considered from the standpoint of genetics. Biological Reviews, 14, 261–280.

    Article  Google Scholar 

  • Muller, H. J. (1942). Isolating mechanisms, evolution, and temperature. Biology Symposium, 6, 71–125.

    Google Scholar 

  • Naisbit, R. E., Jiggins, C. D., Linares, M., Salazar, C., & Mallet, J. (2002). Hybrid sterility, Haldane’s rule and speciation in Heliconius cydno and H. melpomene. Genetics, 161, 1517–1526.

    PubMed  PubMed Central  Google Scholar 

  • Newman, H. (1907). Spawning behavior and sexual dimorphism in Fundulus heteroclitus and allied fish. Biological Bulletin, 12, 314–348.

    Article  Google Scholar 

  • Nosil, P. (2012). Ecological speciation. New York: Oxford University Press.

    Book  Google Scholar 

  • Orr, H. A. (1987). Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics, 116, 555–563.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Orti, G., Bell, M. A., Reimchen, T. E., & Meyer, A. (1994). Global survey of mitochondrial DNA sequences in the threespine Stickleback: Evidence for recent migrations. Evolution, 48, 608–622.

    Article  Google Scholar 

  • Ostevik, K. L., Andrew, R. L., Otto, S. P., & Rieseberg, L. H. (2016). Multiple reproductive barriers separate recently diverged sunflower ecotypes. Evolution, 70, 2322–2335.

    Article  Google Scholar 

  • Panhuis, T. M., Butlin, R., Zuk, M., & Tregenza, T. (2001). Sexual selection and speciation. Trends in Ecology & Evolution, 16, 364–371.

    Article  Google Scholar 

  • Pombi, M., Kengne, P., Gimonneau, G., Tene-Fossog, B., Ayala, D., Kamdem, C., et al. (2017). Dissecting functional components of reproductive isolation among closely related sympatric species of the Anopheles gambiae complex. Evolutionary Applications, 10, 1102–1120.

    Article  Google Scholar 

  • Presgraves, D. C. (2010). Darwin and the origin of interspecific genetic incompatibilities. The American Naturalist, 176, S45–S60.

    Article  Google Scholar 

  • Ramsey, J., Bradshaw, H. D., & Schemske, D. W. (2003). Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution, 57, 1520–1534.

    Article  Google Scholar 

  • Reynolds, J., & Gross, M. (1992). Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proceedings of the Royal Society of London B, 250, 57–62.

    Article  Google Scholar 

  • Rundle, H. D., & Schluter, D. (1998). Reinforcement of stickleback mate preferences: Sympatry breeds contempt. Evolution, 52, 200–208.

    Article  Google Scholar 

  • Salzburger, W., Niederstätter, H., Brandstätter, A., Berger, B., Parson, W., Snoeks, J., et al. (2006). Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proceedings of the Royal Society of London B, 273, 257–66.

    Article  Google Scholar 

  • Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution, 16, 372–380.

    Article  CAS  Google Scholar 

  • Seehausen, O., van Alphen, J., & Witte, F. (1997). Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808–1811.

    Article  CAS  Google Scholar 

  • Seehausen, O., & Van Alphen, J. J. M. (1998). The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behavioral Ecology and Sociobiology, 42, 1–8.

    Article  Google Scholar 

  • Sobel, J. M., & Chen, G. F. (2014). Unification of methods for estimating the strength of reproductive isolation. Evolution, 68, 1511–1522.

    Article  Google Scholar 

  • Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64, 295–315.

    Article  Google Scholar 

  • Taylor, M., Leach, G., & DiMichele, L. (1979). Lunar Spawning Cycle in the Mummichog, Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia 1979, 291–297.

    Article  Google Scholar 

  • Vigueira, P. A., Schaefer, J. F., Duvernell, D. D., & Kreiser, B. R. (2007). Tests of reproductive isolation among species in the Fundulus notatus (Cyprinodontiformes: Fundulidae) species complex. Evolutionary Ecology, 22, 55–70.

    Article  Google Scholar 

  • Whitehead, A. (2010). The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.). Evolution, 64, 2070–2085.

    PubMed  Google Scholar 

  • Williams, T. H., & Mendelson, T. C. (2014). Quantifying reproductive barriers in a sympatric pair of darter species. Evolutionary Biology, 41, 212–220.

    Article  Google Scholar 

  • Zeng, L. W., & Singh, R. S. (1993). The genetic basis of Haldane’s rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. Genetics, 134, 251–260.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank the Lerner-Gray Memorial Fund of the American Museum of Natural History, the UNF Graduate School, and the UNF Coastal Biology Program for providing funding for this research. We thank Carlos Barbas, Jennifer Raabe, Victor Senf, Veronica Logue and Leigh Jordan for their help with collecting and caring for animals. Additionally, we would like to thank Dr. Kelly Smith and Dr. Eric Johnson for their comments on previous versions of this work and to Dr. Elena Buzaianu for statistical suggestions.

Author information

Authors and Affiliations

  1. Department of Biology, University of North Florida, 1 UNF Drive, Jacksonville, FL, 32224, USA

    Ruthie E. Barbas & Matthew R. Gilg

Authors
  1. Ruthie E. Barbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew R. Gilg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew R. Gilg.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 93 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barbas, R.E., Gilg, M.R. Quantification of Reproductive Isolating Barriers Between Two Naturally Hybridizing Killifish Species. Evol Biol 45, 425–436 (2018). https://doi.org/10.1007/s11692-018-9460-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-018-9460-0

Keywords

Search

Navigation