A role for migration-linked genes and genomic islands in divergence of a songbird

Next-generation sequencing has made it possible to begin asking questions about the process of divergence at the level of the genome. For example, recently there has been a debate around the role of “genomic islands of divergence” (i.e. blocks of outlier loci) in facilitating the process of speciation-with-gene-flow. The Swainson’s thrush, Catharus ustulatus, is a migratory songbird with two genetically-distinct subspecies that differ in a number of traits known to be involved in reproductive isolation in birds (plumage coloration, song, and migratory behavior), despite contemporary gene flow along a secondary contact zone. Here we use RAD-PE sequencing to test emerging hypotheses about the process of divergence at the level of the genome and identify genes and gene regions involved in differentiation in this migratory songbird. Our analyses revealed distinct genomic islands on 15 of the 23 chromosomes and levels of differentiation that were 2-3 orders of magnitude higher on the sex chromosomes than the autosomes. Further, an analysis of loci linked to pigmentation, song, and migratory behavior showed that genes linked to migration are significantly more differentiated then expected by chance, but that these genes lie primarily outside of the genomic islands. Overall, our analysis supports the idea that genes linked to migration play an important role in divergence in migratory songbirds, but we find no compelling evidence that the observed genomic islands are facilitating adaptive divergence in migratory behavior.

下一代测序（Next-generation sequencing）技术已为在基因组层面探究物种分化进程提供了可能。例如，近期学界围绕“分化基因组岛（genomic islands of divergence）”——即异常位点（outlier loci）区块——在介导“有基因流动的物种形成（speciation-with-gene-flow）”过程中所发挥的作用展开了广泛争论。斯温氏鸫（Swainson’s thrush，*Catharus ustulatus*）是一种迁徙鸣禽，现存两个遗传分化显著的亚种；尽管二者在次生接触带（secondary contact zone）存在当代基因流，但二者在多项已知与鸟类生殖隔离（reproductive isolation）相关的性状上存在差异，包括羽色、鸣唱及迁徙行为。本研究采用RAD-PE测序（RAD-PE sequencing）技术，针对该迁徙鸣禽的基因组分化进程相关新兴假说开展检验，并鉴定参与物种分化的基因及基因区域。分析结果显示，其23条染色体中有15条存在显著的分化基因组岛；且性染色体上的分化水平较常染色体高出2~3个数量级。进一步针对与色素沉着、鸣唱及迁徙行为相关的位点开展分析后发现，与迁徙相关的基因其分化程度显著高于随机预期，但这类基因主要位于分化基因组岛之外。总体而言，本研究结果支持“与迁徙相关的基因在迁徙鸣禽的物种分化中发挥重要作用”这一观点，但未发现有力证据表明本次观测到的分化基因组岛可促进迁徙行为的适应性分化。