Genomic evidence for correlated trait combinations and antagonistic selection contributing to counterintuitive genetic patterns of adaptive diapause divergence in Rhagoletis flies

<p>Adaptation to novel environments often results in unanticipated genomic responses to selection. Here, we illustrate how multifarious, correlational selection helps explain a counterintuitive pattern of genetic divergence between the recently derived apple- and ancestral hawthorn-infesting host races of <i>Rhagoletis pomonella</i> (Diptera: Tephritidae). The Apple host race terminate diapause and emerge as adults earlier in the season than the hawthorn host race to coincide with the earlier fruiting phenology of their apple hosts. However, alleles at many loci associated with later emergence paradoxically occur at higher frequencies in sympatric populations of the apple than hawthorn race. We present genomic evidence that historical selection over geographically varying environmental gradients across North America generated genetic correlations between two life history traits, diapause intensity and diapause termination, in the hawthorn host race that are strongly associated with genomic regions in high linkage disequilibrium (LD). These genetic correlations are antagonistic to contemporary selection on local apple host race populations for increased initial diapause depth coupled with earlier, not later, diapause termination. Thus, the paradox of apple flies appears due, in part, to pleiotropy or linkage of alleles associated with later adult emergence with increased initial diapause intensity, the latter trait strongly selected for by the earlier phenology of apples. In contrast, loci associated only with diapause termination and not also initial diapause intensity showed the expected pattern (more early-associated alleles in the apple race) in half of sympatric population pairs surveyed. Our results demonstrate how a more complete understanding of multivariate trait combinations and the correlative nature of selective forces acting on them may generally help improve predictions of the genomics of rapid adaptive evolution and explain seemingly counterintuitive patterns of genetic diversity in nature.</p>