Data from: Rapid seasonal evolution in innate immunity of wild Drosophila melanogaster

Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes across a range of taxa. Here, we use immune defence in natural populations of Drosophila melanogaster to understand the rate of evolution in natural populations and the genetics underlying rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect along eastern North America (Massachusetts, Pennsylvania and Virginia). There are pronounced and repeatable changes in the immune response over the approximately 10 generations between spring and autumn collections, with a significant but less distinct difference observed among geographical locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles underlie the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defence in natural populations.

解析演化变化速率与助力快速适应的遗传架构，是演化生物学领域当前的核心挑战之一。比较研究表明，在多个类群中，具备免疫功能的基因属于演化速率最快的基因之列。本研究以黑腹果蝇（Drosophila melanogaster）的自然种群为研究对象，通过分析其免疫防御特征，解析自然种群的演化速率及快速演化背后的遗传机制。我们以北美东部纬度梯度（覆盖马萨诸塞州、宾夕法尼亚州与弗吉尼亚州）按季节时序采集的野生黑腹果蝇种群为材料，利用自然病原体粪肠球菌（Enterococcus faecalis）与雷氏普罗威登斯菌（Providencia rettgeri）侵染果蝇，以此测定其感染后的存活率与细菌载量。在春、秋两季采样间隔的约10个世代中，果蝇的免疫应答出现了显著且可重复的变化；不同地理种群间虽存在显著差异，但差异程度相对较弱。尽管在随季节周期性变化的等位基因中，并未富集已知免疫功能基因，但我们通过构建重组远交种群，对免疫基因中部分随季节周期性波动的等位基因的功能进行了验证。研究发现，携带硫酯蛋白3（Thioester-containing protein 3, Tep3）季节性等位基因的果蝇，其感染后的功能应答存在显著差异；且季节性Tep3等位基因与果蝇抗菌肽类似蛋白6（Drosomycin-like 6, Dro6）等位基因之间的上位性互作，是自然种群中观测到的免疫表型的成因。这种针对季节性环境压力的快速周期性免疫应答，加深了我们对调控自然种群免疫防御演化的复杂生态与遗传互作机制的认知。