Abstract

Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Although this process is a major generator of biodiversity, its genetic basis is still poorly understood. Here we investigate the genetic architecture of niche differentiation in a sympatric species pair of threespine stickleback fish by mapping the environment-dependent effects of phenotypic traits on hybrid feeding and performance under semi-natural conditions. We show that multiple, unlinked loci act largely additively to determine position along the major niche axis separating these recently diverged species. We also find that functional mismatch between phenotypic traits reduces the growth of some stickleback hybrids beyond that expected from an intermediate phenotype, suggesting a role for epistasis between the underlying genes. This functional mismatch might lead to hybrid incompatibilities that are analogous to those underlying intrinsic reproductive isolation but depend on the ecological context.

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Acknowledgements

We thank J. Perez for counting gill rakers; C. Sather for performing lab work for SNP genotyping; and K. Broman, G. Coop, I. Goodliffe, A. Greenwood, P. Wainwright, M. White and M. Wund for constructive comments. Stable isotopes were analysed at the University of California, Davis, Stable Isotope Facility. Funding was provided by grants from the US National Institutes of Health (F32 GM086125 to M.E.A., R01 GM089733 to C.L.P. and D.S., and P50 HG002568 to C.L.P. and D.M.K.), the Natural Sciences and Engineering Research Council of Canada (to D.S.) and the Canada Foundation for Innovation (to D.S.).

Author information

Author notes

    • Sara Bergek

    Present address: Swedish University of Agricultural Sciences, Department of Aquatic Resources, Stångholmsvägen 2, SE-17893 Drottningholm, Sweden.

Affiliations

  1. Fred Hutchinson Cancer Research Center, Human Biology and Basic Sciences Divisions, 1100 Fairview Avenue North, Seattle, Washington 98109, USA

    • Matthew E. Arnegard
    •  & Catherine L. Peichel
  2. University of British Columbia, Biodiversity Research Centre and Zoology Department, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada

    • Matthew E. Arnegard
    • , Kerry B. Marchinko
    • , Gina L. Conte
    • , Sahriar Kabir
    • , Nicole Bedford
    •  & Dolph Schluter
  3. University of California at Davis, Department of Evolution and Ecology, One Shields Avenue, Davis, California 95616, USA

    • Matthew D. McGee
  4. EAWAG, Department of Aquatic Ecology, Center for Ecology, Evolution, and Biogeochemistry, Seestrasse 79, 6047 Kastanienbaum, Switzerland

    • Blake Matthews
  5. Uppsala University, Department of Animal Ecology, Evolutionary Biology Centre (EBC), Norbyvägen 18D, SE-75236 Uppsala, Sweden

    • Sara Bergek
  6. Stanford University School of Medicine, Department of Developmental Biology and Howard Hughes Medical Institute, 279 Campus Drive, Stanford, California 94305, USA

    • Yingguang Frank Chan
    • , Felicity C. Jones
    •  & David M. Kingsley

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Contributions

M.E.A., C.L.P. and D.S. designed, planned and oversaw the project. M.E.A. made the crosses, set up the experimental pond and coordinated all field and laboratory research. M.E.A., K.B.M., S.K., N.B. and S.B. conducted fieldwork and stable-isotope analysis. M.D.M. measured functional morphological traits. B.M. and M.E.A. measured and analysed gut contents. S.K., D.S. and M.E.A. performed landmark-based morphometric analyses. M.E.A. analysed relationships between all traits and trophic variation. F.C.J., Y.F.C. and D.M.K. designed the SNP genotyping array. M.E.A., G.L.C., C.L.P and D.S. analysed SNP genotypes. D.S. determined the genealogy of the mapping population on the basis of SNP genotypes. M.E.A., C.L.P. and D.S. performed linkage and QTL analysis. M.E.A., C.L.P. and D.S. tested the genetic architecture of niche divergence. M.E.A., C.L.P., D.S., M.D.M., B.M. and G.L.C. interpreted the results. M.E.A. wrote the paper with input from C.L.P. and D.S., who are co-senior authors. All other authors provided editorial comments and approved the final version of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Matthew E. Arnegard.

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https://doi.org/10.1038/nature13301

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