Data from: Genome-wide evidence for speciation with gene flow in Heliconius butterflies

Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on whole genome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100 kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Müllerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.

绝大多数物种形成事件大概率以渐进方式发生，并未形成完全且即时的生殖隔离（reproductive isolation），但分化物种间基因流（gene flow）的完整规模，极少能在全基因组（genome-wide）尺度上得到精准刻画。量化分化物种间基因渐渗（admixture）的范围与发生时机，有助于阐明地理隔离在物种形成过程中所发挥的作用。本研究基于31个个体的全基因组测序数据，采用全新分析方法对袖蝶属（Heliconius）蝴蝶不同分化阶段的基因渐渗水平开展定量测定。对红带袖蝶（H. melpomene）、诗袖蝶（H. cydno）与提姆袖蝶（H. timareta）的同域（sympatric）种群与异域（allopatric）种群进行比较后发现，同域种群间存在全基因组水平的共享变异增多趋势，这表明物种间存在广泛的跨物种基因流。在100kb的基因组窗口（genomic windows）中，多达40%的窗口按地理来源而非物种进行聚类，这证明同域分布的物种间共享了相当比例的基因组序列。对不同时间尺度下共享的遗传变异进行分析后发现，这些物种间的基因渐渗自物种形成早期便持续发生。近期共享的等位基因所展现的连锁不平衡（linkage disequilibrium）水平，高于长期共享的等位基因，这说明该基因渐渗事件在物种分化进程中多次发生，且目前可能仍在持续。在调控翅型分化的基因座（loci）附近，以及整条Z染色体（Z chromosome）区域，基因渐渗信号均显著减弱，这与缪氏拟态（Müllerian mimicry）的强选择压力以及已知的Z染色体连锁杂交不亲和（hybrid incompatibility）现象相符。综合上述结果可知，即便在长期持续且遍及全基因组的基因渐渗背景下，物种分化依然可以顺利完成。