Hybrid dysgenesis in Drosophila simulans associated with a rapid invasion of the P-element

In a classic example of the invasion of a species by a selfish genetic element, the P-element was horizontally transferred from a distantly related species into Drosophila melanogaster. Despite causing ‘hybrid dysgenesis’, a syndrome of abnormal phenotypes that include sterility, the P-element spread globally in the course of a few decades in D. melanogaster. Until recently, its sister species, including D. simulans, remained P-element free. Here, we find a hybrid dysgenesis-like phenotype in the offspring of crosses between D. simulans strains collected in different years; a survey of 181 strains shows that around 20% of strains induce hybrid dysgenesis. Using genomic and transcriptomic data, we show that this dysgenesis-inducing phenotype is associated with the invasion of the P-element. To characterize this invasion temporally and geographically, we survey 631 D. simulans strains collected on three continents and over 27 years for the presence of the P-element. We find that the D. simulans P-element invasion occurred rapidly and nearly simultaneously in the regions surveyed, with strains containing P-elements being rare in 2006 and common by 2014. Importantly, as evidenced by their resistance to the hybrid dysgenesis phenotype, strains collected from the latter phase of this invasion have adapted to suppress the worst effects of the P-element.

作为自私遗传元件侵染物种的经典案例，P因子（P-element）从远缘物种经水平转移进入黑腹果蝇（Drosophila melanogaster）。尽管其会引发“杂种不育综合征（hybrid dysgenesis）”——一类涵盖不育在内的异常表型综合征，但P因子仅用数十年便在黑腹果蝇种群中实现全球扩散。直至近期，其姊妹物种如拟暗果蝇（Drosophila simulans）等始终未被P因子侵染。本研究发现，不同年份采集的拟暗果蝇品系杂交后代中出现了类似杂种不育综合征的表型；对181个品系的调查显示，约20%的品系可诱导杂种不育综合征。借助基因组数据（genomic data）与转录组数据（transcriptomic data），我们证实该不育诱导表型与P因子的侵染存在关联。为从时间与地理维度表征此次侵染过程，我们对采集自三大洲、跨度27年的631个拟暗果蝇品系开展P因子携带情况检测。结果显示，拟暗果蝇的P因子侵染发生迅速且在各调查区域近乎同步：2006年携带P因子的品系仍极为罕见，至2014年已极为普遍。尤为关键的是，从该侵染后期采集的品系已演化出对杂种不育综合征的抗性，这表明它们已适应并抑制了P因子带来的最严重危害。