Organisms living in seasonally variable environments utilize cues such as light and temperature to induce plastic responses, enabling them to exploit favorable seasons and avoid unfavorable ones. Local adapation can result in variation in seasonal responses, but the genetic basis and evolutionary history of this variation remains elusive. Many insects, including Drosophila melanogaster, are able to undergo an arrest of reproductive development (diapause) in response to unfavorable conditions. In D. melanogaster, the ability to diapause is more common in high latitude populations, where flies endure harsher winters, and in the spring, reflecting differential survivorship of overwintering populations. Using a novel hybrid swarm-based genome wide association study, we examined the genetic basis and evolutionary history of ovarian diapause. We exposed outbred females to different temperatures and day lengths, characterized ovarian development for over 2800 flies, and reconstructed their complete, phased genomes. We found that diapause, scored at two different developmental cutoffs, has modest heritability, and we identified hundreds of SNPs associated with each of the two phenotypes. Alleles associated with one of the diapause phenotypes tend to be more common at higher latitudes, but these alleles do not show predictable seasonal variation. The collective signal of many small-effect, clinally varying SNPs can plausibly explain latitudinal variation in diapause seen in North America. Alleles associated with diapause are segregating in Zambia, suggesting that variation in diapause relies on ancestral polymorphisms, and both pro- and anti-diapause alleles have experienced selection in North America. Finally, we utilized outdoor mesocosms to track diapause under natural conditions. We found that hybrid swarms reared outdoors evolved increased propensity for diapause in late fall, whereas indoor control populations experienced no such change. Our results indicate that diapause is a complex, quantitative trait with different evolutionary patterns across time and space.

生活在季节性变化环境中的生物体利用光和温度等线索来诱导可塑性反应，使它们能够利用有利的季节并避开不利的季节。局部适应可能导致季节性反应的变化，但这种变化的遗传基础和进化历史仍然难以捉摸。许多昆虫，包括果蝇，能够因不利条件而停止生殖发育（滞育）。在D中。黑腹果蝇的滞育能力在高纬度种群中更为常见，在那里，果蝇经历了更严酷的冬天，而在春天，反映了越冬种群的不同存活率。使用一种新型的基于杂交群的全基因组关联研究，我们检查了卵巢滞育的遗传基础和进化历史。我们将远交系雌性果蝇暴露在不同的温度和日照长度下，对 2800 多只果蝇的卵巢发育进行了表征，并重建了它们完整的、分阶段的基因组。我们发现，在两个不同的发育截止点评分的滞育具有适度的遗传力，并且我们鉴定了数百个与这两种表型相关的 SNP。与滞育表型之一相关的等位基因往往在高纬度地区更常见，但这些等位基因没有表现出可预测的季节性变化。许多小效应、临床变化的 SNP 的集体信号可以合理地解释北美滞育的纬度变化。与滞育相关的等位基因在赞比亚发生分离，表明滞育的变异依赖于祖先的多态性，并且亲滞育和反滞育等位基因在北美都经历了选择。 最后，我们利用室外中生态系统来追踪自然条件下的滞育。我们发现，在室外饲养的混合群在深秋时滞育的倾向增加，而室内对照种群则没有经历这种变化。我们的结果表明，滞育是一种复杂的数量性状，在时间和空间上具有不同的进化模式。