Data from: Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction-site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small Ne (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome-wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Ne in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.

长久以来，驱动岛屿形成极其丰富生物多样性的演化机制一直深受演化生物学家的关注。研究表明，岛屿环境中遗传漂变（genetic drift）与趋异选择（divergent selection）的作用强度往往较高，二者均可推动种群分化（population divergence）与物种形成（speciation）；但另一方面，强烈的遗传漂变也可能阻碍种群的适应性演化。本研究针对岛屿灰狐（Urocyon littoralis）开展基因组分析（genomic analysis），以检验遗传漂变与趋异选择在该物种种群间遗传分化中的作用。该物种共计6个亚种（subspecies），每个亚种均栖息于加利福尼亚海峡群岛（California Channel Islands）的不同岛屿之上。本研究对通过限制性酶切位点相关DNA（Restriction-site Associated DNA, RAD）测序获得的5293个单核苷酸多态性（Single Nucleotide Polymorphism, SNP）位点进行分析，结果支持遗传漂变是驱动岛屿灰狐种群分化的主导演化机制。具体而言，各岛屿灰狐种群的遗传变异水平极低，有效种群大小（effective population size, Ne）介于2.1至89.7之间（中位数为19.4），且存在显著的种群瓶颈（population bottleneck）遗传信号。此外，遗传变异水平最低（据此可推测历史上遗传漂变作用最强）的岛屿种群，与大陆灰狐的遗传分化程度也最高，反之亦然，这表明遗传漂变推动了全基因组水平的种群分化。不过，异常位点检测（outlier tests）将3.6%至6.6%的位点鉴定为高固定指数（Fixation Index, FST）异常位点，这表明尽管遗传漂变作用强烈，趋异选择仍对种群分化存在贡献。基于高FST异常位点得出的种群相似性模式，与基于形态学（morphology）特征得出的模式高度吻合，为异常位点反映适应性分化提供了额外证据。部分岛屿灰狐种群（尤其是圣尼古拉斯岛（San Nicolas Island）种群）的遗传变异水平极低且有效种群规模极小，这意味着它们极易发生有害等位基因（deleterious alleles）的固定、适合度（fitness）下降以及适应性潜能（adaptive potential）降低。