Genetic evidence for environment-dependent hybrid incompatibilities in threespine stickleback

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 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 (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci—a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

Genomic insights into variation in thermotolerance between hybridizing swordtail fishes

“…Together, this work highlights the potential for ecological incompatibilities to play a role in selection on X. malinche-X. birchmanni hybrids [46]. Nearly a decade of work has uncovered evidence for genetic incompatibilities between these two species, but most cases that have been evaluated in detail have focused on intrinsic hybrid incompatibilities [89,127].…”

“…Recently attention has been paid to regulatory BDMIs, which arise from the coevolution of cis and trans regulatory elements within species that become mismatched and cause misexpression of target genes in hybrids [1,36,43,44] (here, misexpression is defined as expression of genes in hybrids that is much higher or lower than that observed in either parent species). BDMIs can impact a range of traits, including those relevant for an individual's survival in their environment [45,46]. In fact, both theory and empirical results suggest that BDMIs may frequently arise from divergent adaptation to the environment [47][48][49].…”

“…In fact, both theory and empirical results suggest that BDMIs may frequently arise from divergent adaptation to the environment [47][48][49]. In addition to the expectation that hybrids may have reduced ecological fitness due to phenotypic intermediacy or dominance of particular parental traits [45,46,[50][51][52][53][54], BDMIs can arise at loci underlying ecological traits. Despite their predicted importance, few ecological BDMIs have been identified to date [46] (see [55] and [46] for examples from Arabidopsis and sticklebacks), making it difficult to study the tradeoffs between adaptive introgression of ecological traits and selection on ecological BDMIs in hybrids.…”

“…In addition to the expectation that hybrids may have reduced ecological fitness due to phenotypic intermediacy or dominance of particular parental traits [45,46,[50][51][52][53][54], BDMIs can arise at loci underlying ecological traits. Despite their predicted importance, few ecological BDMIs have been identified to date [46] (see [55] and [46] for examples from Arabidopsis and sticklebacks), making it difficult to study the tradeoffs between adaptive introgression of ecological traits and selection on ecological BDMIs in hybrids. An ecological trait that can be used to address this gap and that is of particular interest for predicting how populations may adapt to global climate change is thermal tolerance [56][57][58].…”

Genomic insights into variation in thermotolerance between hybridizing swordtail fishes

“…BDMIs can impact a range of traits, including those relevant for an individual’s survival in their environment [45,46]. In fact, both theory and empirical results suggest that BDMIs may frequently arise from divergent adaptation to the environment [47–49].…”