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Cryptic gametic interactions confer both conspecific and heterospecific advantages in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone

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Abstract

Most species pairs are isolated through the collective action of a suite of barriers. Recent work has shown that cryptic barriers such as conspecific sperm precedence can be quite strong, suggesting that they evolve quickly. However, because the strength of multiple barriers has been formally quantified in very few systems, the relative speed with which conspecific sperm precedence evolves remains unclear. Here, we measure the strength of both conspecific sperm precedence and cryptic non-competitive isolation between the hybridizing sister species, Chrysochus auratus and C. cobaltinus (Coleoptera: Chrysomelidae), and compare the strength of those barriers to the strength of other known reproductive barriers in this system. Overall, cryptic barriers in this system are weaker than other barriers, indicating that they have not evolved rapidly. Furthermore, their evolution has been asymmetric. Non-competitive barriers substantially reduce the production of hybrid offspring by C. auratus females but not by C. cobaltinus females. In multiply-mated C. cobaltinus females, heterospecific sperm outcompete conspecific sperm, as evidenced by the fact that heterospecific males sired disproportionately more offspring than predicted from the results for singly-mated females. In C. auratus females, neither sperm type has a competitive advantage. Such asymmetries explain why nearly all F1 hybrids in the field are from crosses between C. cobaltinus females and C. auratus males. We discuss these findings in terms of understanding the cost of mating ‘mistakes’ in the Chrysochus hybrid zone. In addition, our discovery that 95% confidence intervals for commonly-used isolation statistics can be very wide has important implications for speciation research. Specifically, to avoid biases in the interpretation of such isolation metrics, we suggest that studies should routinely include error estimates in their analyses of reproductive isolation.

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Acknowledgments

This work would not have been possible without the assistance of many others, both in the lab and the field, to whom we are grateful. In particular, Timm Beeman, Tyler Bourcier, Monique Brewer, Jabin Green, Liam Hahn, Karina Helm, Barb Honchak, Stefanie Locke, Tracy McFarland, Jessica Mendoza, Meaghan McNeal, Amy Savage, Steven Schwartz, Erik Walker, and Carol Yoon helped collect virgin beetles, perform crosses, and conduct beetle husbandry. In addition, Jillian Bearden, Erin Beardsley, Theresa Black, Barb Honchak, Hallie Kerins, Flordeliza Lilagan, and Joe Skillman assisted with larval genotyping. We are also grateful to Ben Miner for help with the bootstrap analysis, and Doug Schemske and Carol Yoon for stimulating discussions on the ideas discussed herein. Funding for this research was provided by the Biology Department and Office of Research and Sponsored Programs at Western Washington University and the National Science Foundation (DEB-0212652), including supplemental National Science Foundation funding to establish a summer internship, Minority Opportunities for Research on Evolution, in which several of this paper’s coauthors participated. Finally, the first two authors, both of whom have had the privilege of working under the advisement of Rick Harrison, thank Rick for the inspiration to conduct research in hybrid zones and for his unflagging support and encouragement.

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Author notes

  1. Erica L. Larson

    Present address: Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA

  2. Margaret Brassil

    Present address: Department of Immunology, University of Washington, Seattle, WA, 98195, USA

  3. Kati J. Buckingham

    Present address: Department of Pediatrics, University of Washington, Seattle, WA, 98195, USA

  4. Danielle Juárez

    Present address: School of Dentistry, University of Washington, Seattle, WA, 98195, USA

  5. Joseph Deas

    Present address: Department of Entomology, University of Arizona, Tucson, AZ, 85721, USA

  6. Michael A. White

    Present address: Laboratory of Genetics, University of Wisconsin, 425 Henry Mall, Madison, WI, 53706, USA

  7. Jonathan Maslan

    Present address: Wake Forest University School of Medicine, Winston-Salem, NC, 27157, USA

  8. Kirsten J. Monsen

    Present address: Department of Biology and Molecular Biology, Montclair State University, Montclair, NJ, 07043, USA

Authors and Affiliations

  1. Biology Department, Western Washington University, Bellingham, WA, 98225, USA

    Merrill A. Peterson, Erica L. Larson, Margaret Brassil, Kati J. Buckingham, Danielle Juárez, Michael A. White, Jonathan Maslan, Andrew Schweitzer & Kirsten J. Monsen

  2. Department of Biology, San Diego State University, San Diego, CA, 92182, USA

    Joseph Deas

  3. Department of Biology, California State University, Northridge, CA, 91330, USA

    Donna Mangloña

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  1. Merrill A. Peterson
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Correspondence to Merrill A. Peterson.

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Peterson, M.A., Larson, E.L., Brassil, M. et al. Cryptic gametic interactions confer both conspecific and heterospecific advantages in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone. Genetica 139, 663–676 (2011). https://doi.org/10.1007/s10709-011-9567-z

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