Concurrent starling invasions suggest selection on shared genomic regions even after genetic bottlenecks

A species' success during the invasion of new areas hinges on an interplay between the demographic processes common to invasions and the specific ecological context of the novel environment. Evolutionary genetic studies of invasive species can investigate how genetic bottlenecks and ecological conditions shape genetic variation in invasions, and our study pairs two invasive populations that are hypothesized to be from the same source population to compare how each population evolved during and after introduction. Invasive European Starlings (Sturnus vulgaris) established populations in both Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European Starling populations from three continents to determine howdemographic processes interact with rapid evolution to generate similar genetic patterns in these recent and replicated invasions. Demographic models indicate that both invasive populations experienced genetic bottlenecks, and we find that specific genomic regions have differentiated even on this short evolutionary timescale. Despite these bottlenecks, we suggest that genetic drift alone cannot explain differentiation in at least two of these regions, given that within-population nucleotide diversity and neutrality statistics indicate a role for purifying and/or diversifying selection. Instead, the patterns of genetic variation we find are consistent with the hypothesis that this infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors), perhaps in part due to the demographic boom intrinsic to many invasions.

一个物种在入侵新区域时的成功与否，取决于两类因素的相互作用：一类是各类入侵事件共有的种群统计过程，另一类是新环境的特定生态背景。入侵物种的进化遗传学（Evolutionary genetics）研究可揭示遗传瓶颈（genetic bottleneck）与生态条件如何塑造入侵过程中的遗传变异；本研究选取两个被推测源自同一源种群（source population）的入侵种群，对比二者在引种过程中及引种后的演化路径。入侵的欧洲椋鸟（European Starling，Sturnus vulgaris）于19世纪在澳大利亚与北美建立了野生种群。本研究对来自三大洲的本土种群与独立引种的欧洲椋鸟种群开展全基因组序列（whole-genome sequences）比对分析，以阐明种群统计过程与快速演化如何相互作用，在这两个新近发生且可重复的入侵事件中催生相似的遗传模式。种群统计模型显示，两个入侵种群均经历了遗传瓶颈；同时我们发现，即便在如此短暂的演化时间尺度内，部分特定基因组区域已发生分化。尽管存在上述遗传瓶颈，但我们认为仅靠遗传漂变（genetic drift）无法解释其中至少两个区域的分化——种群内核苷酸多样性（nucleotide diversity）与中性统计检验（neutrality statistics）结果表明，净化选择（purifying selection）和/或歧化选择（diversifying selection）发挥了作用。与之相反，我们观测到的遗传变异模式与下述假说一致：这一臭名昭著且移动能力极强的入侵物种能够适应新的选择压力（例如外在环境因素），而这一适应过程可能部分得益于多数入侵事件所固有的种群爆发式增长（demographic boom）。