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. We have quantified admixture and genetic differentiation genome-wide at different stages of divergence in the neotropical butterfly genus Heliconius, by sequencing the whole genomes of 31 individuals. Comparisons between sympatric and allopatric populations of sister species H. melpomene and members of the H. cydno/timareta group 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. Estimation of admixture at different levels of phylogenetic divergence indicated that gene flow between these species has continued since early in speciation. The level of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection on Müllerian mimicry and known Z-linked hybrid incompatibility. Overall these results show that ecologically divergent species can emerge and persist despite ongoing gene flow affecting a surprisingly large fraction of the genome.

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，但目前极少有研究能在全基因组尺度上，刻画分化物种间基因流的完整规模。明确分化物种间基因渐渗(admixture)的范围与时间，能够阐明地理隔离在物种形成过程中的作用。本研究通过对31个个体进行全基因组测序，对新热带区袖蝶属（Heliconius）不同分化阶段的全基因组基因渐渗与遗传分化进行了定量分析。通过对姐妹物种红带袖蝶（H. melpomene）与H. cydno/timareta类群的同域分布(sympatric)与异域分布(allopatric)种群开展比较，研究团队发现同域种群间呈现全基因组共享变异增加的整体趋势，表明二者间存在广泛的种间基因流。多达40%的100 kb基因组窗口按地理来源而非物种聚类，证实同域物种间共享了占比可观的基因组片段。对不同系统发育分化水平下的基因渐渗进行估算后发现，这些物种间的基因流自物种形成早期便持续存在。在控制趋异翅型的基因位点周围以及整条Z染色体上，基因渐渗水平均显著降低，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性的研究结论相符。综上，本研究结果表明，尽管持续的基因流影响了比例惊人的基因组片段，但生态趋异的物种仍可形成并维持存续。