Spatiotemporal dynamics and genome-wide association analysis of desiccation tolerance in Drosophila melanogaster

Water availability is a major environmental challenge to a variety of terrestrial organisms. In insects, desiccation tolerance varies predictably over spatial and temporal scales and is an important physiological determinant of fitness in natural populations. Here, we examine the dynamics of desiccation tolerance in North American populations of Drosophila melanogaster using: 1) natural populations sampled across latitudes and seasons; 2) experimental evolution in field mesocosms over seasonal time; 3) genome-wide associations to identify SNPs/genes associated with variation for desiccation tolerance; and 4) subsequent analysis of patterns of clinal/seasonal enrichment in existing pooled sequencing data of populations sampled in both North America and Australia. A cline in desiccation tolerance was observed, for which tolerance exhibited a positive association with latitude; tolerance also varied predictably with culture temperature, demonstrating a significant degree of thermal plasticity. Desiccation tolerance evolved rapidly in field mesocosms, although only males showed differences in desiccation tolerance between spring and autumn collections from natural populations. Water loss rates did not vary significantly among latitudinal or seasonal populations; however, changes in metabolic rates during prolonged exposure to dry conditions are consistent with increased tolerance in higher latitude populations. Genome wide associations in a panel of inbred lines identified twenty-five SNPs in twenty-one loci associated with sex-averaged desiccation tolerance, but there is no robust signal of spatially varying selection on genes associated with desiccation tolerance. Together, our results suggest that desiccation tolerance is a complex and important fitness component that evolves rapidly and predictably in natural populations.

水分可获得性是诸多陆生生物面临的主要环境挑战之一。在昆虫中，脱水耐受性（desiccation tolerance）随空间与时间尺度呈现可预测的变化，是自然种群中适合度的重要生理决定因素。本研究以北美种群的黑腹果蝇（Drosophila melanogaster）为对象，通过以下四种方式探究其脱水耐受性的动态变化：1）对跨纬度与季节采集的自然种群进行分析；2）在野外中型实验生态系统（field mesocosms）中开展季节性周期的实验演化研究；3）借助全基因组关联分析，鉴定与脱水耐受性变异相关的单核苷酸多态性（SNPs）及基因；4）对北美与澳大利亚两地采集种群的现有混合测序数据进行后续分析，以探究其梯度分布/季节性富集模式。研究观察到脱水耐受性存在纬度梯度变异：耐受性与纬度呈正相关；同时耐受性随培养温度呈现可预测的变化，表明其具备显著程度的热可塑性。脱水耐受性在野外中型实验生态系统中演化迅速，但仅在雄性个体中观察到自然种群春季与秋季采集样本的脱水耐受性差异。不同纬度或季节的种群间，水分流失速率无显著差异；但在长期暴露于干燥环境的过程中，代谢速率的变化与高纬度种群更高的脱水耐受性相一致。对一组近交系（inbred lines）开展的全基因组关联分析，在21个基因座中鉴定出25个与性别平均脱水耐受性相关的单核苷酸多态性，但未发现与脱水耐受性相关基因存在空间异质性选择的可靠信号。综合来看，本研究结果表明，脱水耐受性是一类复杂且重要的适合度组成部分，可在自然种群中快速且可预测地发生演化。