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.

对新环境的适应往往会引发难以预判的基因组水平选择响应。本文阐释了多维度相关选择如何帮助解释苹果实蝇（Rhagoletis pomonella，双翅目（Diptera）实蝇科（Tephritidae））新近衍生的寄生苹果宿主宗与祖先型寄生山楂宿主宗之间存在的反直觉遗传分化模式。苹果宿主宗的个体滞育（diapause）结束并羽化为成虫的时间早于山楂宿主宗，以匹配其寄主苹果更早的结果物候（phenology）。然而，许多与成虫羽化延迟相关的基因座（locus，复数形式loci）的等位基因，在苹果宿主宗的同域种群（sympatric populations）中出现的频率却反常地高于山楂宿主宗。我们提供基因组证据表明，北美范围内地理异质环境梯度下的历史选择，在山楂宿主宗中造就了两种生活史性状——滞育强度与滞育结束——之间的遗传相关，且该相关与处于高连锁不平衡（linkage disequilibrium，LD）的基因组区域紧密关联。这些遗传相关与当地苹果宿主宗种群当前所受的选择压力相悖：苹果宿主宗种群受到的选择倾向于提升初始滞育深度，并使滞育结束时间提前而非延后。因此，苹果实蝇的这一反常现象，部分源于与成虫羽化延迟相关的等位基因存在多效性（pleiotropy），或是与初始滞育强度提升相关的等位基因发生了连锁——而后者性状正被苹果更早的物候所强烈选择。与之相反，仅与滞育结束相关、而非同时关联初始滞育强度的基因座，在本次调研的一半同域种群对中呈现出预期模式：苹果宿主宗中拥有更多与羽化提前相关的等位基因。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压力的相关作用本质，将普遍有助于提升对快速适应性进化基因组学的预测能力，并解释自然界中看似反直觉的遗传多样性模式。