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

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

doi:10.1371/journal.pbio.3001469

Abstract

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.

Highlights

In support of our prediction, mean individual excess ancestry heterozygosity—the deviation from Hardy–Weinberg expectations based on the relative frequency of alternative ancestry alleles in the genome—was significantly elevated among pond-raised fish compared to aquarium-raised fish
Patterns were similar for all studies in the dataset—each study that contributed data from pond experiments found significant excess ancestry heterozygosity, and each study that contributed data from aquaria found that excess ancestry heterozygosity did not differ from 0 (Fig 2B)
We found that excess ancestry heterozygosity was elevated in recombinant stickleback hybrids raised in experimental ponds compared to those from similar crosses raised in aquaria

Summary

Methods

We used both previously published and unpublished data in our analyses. We base our main inference on a comparison of ancestry heterozygosity in hybrids born and raised in aquaria to hybrids from the same cross types born and raised in experimental ponds, which are seminatural ecosystems. See [11,30] for additional information about ponds. Pond-raised crosses capture both “intrinsic” and “extrinsic” incompatibilities, whereas aquarium-raised crosses are expected to capture “intrinsic” incompatibilities that impact hybrid fitness. F2 hybrids were produced via mating between full siblings in both the lab and field

Results

Discussion

Conclusion