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

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 Rhagoletis pomonella (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.生物对新生环境的适应往往会引发意料之外的基因组选择响应。本文阐释了多重相关选择如何帮助解释新近演化出的苹果寄生寄主宗（host race）与祖先山楂寄生寄主宗苹果实蝇（Rhagoletis pomonella，双翅目（Diptera）：实蝇科（Tephritidae））之间存在的反直觉遗传分化模式。苹果寄生寄主宗实蝇的滞育（diapause）终止更早，成虫羽化时间早于山楂寄生寄主宗，以匹配其寄主苹果树更早的结果物候期。但矛盾的是，诸多与较晚成虫羽化相关的等位基因，在同域（sympatric）分布的苹果寄生寄主宗种群中的频率反而高于山楂寄生寄主宗种群。我们提供的基因组证据显示，北美各地理梯度环境下的历史选择，在山楂寄生寄主宗种群中塑造了滞育强度（diapause intensity）与滞育终止（diapause termination）两个生活史性状间的遗传相关，该相关与高度连锁不平衡（linkage disequilibrium, LD）的基因组区域紧密关联。这类遗传相关与当前当地苹果寄生寄主宗种群的选择压力相悖：苹果寄生寄主宗种群被选择获得更深的初始滞育深度，搭配更早而非更晚的滞育终止。因此，苹果实蝇的这一矛盾现象，部分源于与较晚成虫羽化相关的等位基因同时具备多效性（pleiotropy），或与提升初始滞育强度的等位基因存在连锁——而后者恰好被苹果树更早的物候期强烈选择。与之相反，仅与滞育终止相关、未关联初始滞育强度的基因座，在半数调查的同域种群对中呈现了预期模式（苹果寄生寄主宗种群中拥有更多与较早羽化相关的等位基因）。本研究结果表明，若能更全面地理解多变量性状组合及其所受选择的相关作用本质，将有助于更精准地预测快速适应性演化的基因组机制，并解释自然界中看似反直觉的遗传多样性模式。