Analysis of ancestry heterozygosity suggests that hybrid incompatibilities in threespine stickleback are environment dependent

Ken A. Thompson, Catherine L. Peichel, Diana J. Rennison, Matthew D. McGee, Arianne Y.K. Albert, Timothy H. Vines, Anna K. Greenwood, Abigail R. Wark, Yaniv Brandvain, Molly Schumer, Dolph Schluter

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Hybrid incompatibilities occur when interactions between opposite : ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are “intrinsic,” meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.

Original languageEnglish (US)
Article numbere3001469
JournalPLoS biology
Issue number1
StatePublished - Jan 2022

Bibliographical note

Funding Information:
The authors received no specific funding for this work. Feedback from D. Irwin, S. Otto, L. Rieseberg, and R. Stelkens improved the manuscript. Discussions with the Schluter Lab at the University of British Columbia and the Schumer Lab at Stanford University improved the analysis. We are grateful to the authors of the primary studies from which we gathered data for their data stewardship.

Publisher Copyright:
Copyright: © 2022 Thompson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


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