The Genomic Landscape of Divergence Across the Speciation Continuum in an Island-colonising Bird. The genomic landscape of silvereye divergence

Understanding the drivers of global diversity patterns requires knowledge of evolutionary dynamics that transform undifferentiated taxa into reproductively isolated species. A goal of genomic-era analyses is to compare the genomes of diverging forms, and from the distribution of their genomic differences – their genomic landscape of divergence – infer the evolutionary dynamics at play. However, empirical assessment of genomic landscape dynamics across a speciation continuum under varying evolutionary scenarios are few, limiting the ability to achieve this goal. Here we evaluate how divergence accumulates across the genomic landscape in a naturally replicated system that serves as a proxy for the speciation continuum – island colonisations by the silvereye (Zosterops lateralis). Using reduced representation sequencing of comparisons matched for divergence timeframe and gene flow scenario, we document how genomic patterns accumulate as divergence progresses and demonstrate the role of gene flow in slowing the pace of divergence. We found limited support for the idea that divergence accumulates around loci under divergent selection. While a small number of genomic islands were found in populations diverging with and without gene flow, in only one case were SNPs tightly associated with a genomic island, and nor did genomic islands widen with time. Furthermore, the transition from localised to genome-wide levels of divergence was captured with an individual-based simulation model that considered only neutral processes. Our results challenge the ubiquity of verbal models that explain the progression of genomic differences across the speciation continuum by invoking initial divergence at selected loci, and subsequent divergence at adjacent linked loci.

要解析全球生物多样性格局的驱动机制，需阐明将未分化类群转变为生殖隔离物种的进化动力学（evolutionary dynamics）过程。基因组学时代分析的核心目标之一，是比对不同分化类群的基因组，并通过其基因组差异的分布模式——即分化基因组景观（genomic landscape of divergence）——推断当前发挥作用的进化动力学。然而，在不同进化场景下，针对贯穿物种形成连续体（speciation continuum）各阶段的分化基因组景观动态的实证评估仍较为匮乏，这极大限制了该研究目标的实现。

本研究以银绣眼鸟（Zosterops lateralis）的岛屿定殖事件这一自然重复实验系统作为物种形成连续体的替代研究模型，解析分化如何在分化基因组景观中逐步积累。本研究通过对匹配了分化时间尺度与基因流（gene flow）场景的种群样本开展简化基因组测序（reduced representation sequencing），阐明了随着分化进程推进，基因组分化模式的积累规律，并证实了基因流可有效减缓分化速率。

我们发现，“分化会在受歧化选择（divergent selection）的基因座周围积累”这一经典假说仅得到有限支持。尽管在存在基因流与不存在基因流的分化种群中均发现了少量基因组岛（genomic island），但仅在一个案例中发现单核苷酸多态性（Single Nucleotide Polymorphisms, SNPs）与基因组岛存在紧密关联，且基因组岛并未随时间推移而扩大。此外，仅考虑中性过程的个体水平模拟模型，可准确复现从局部分化到全基因组分化的转变过程。

本研究结果对现有主流文字阐释模型的普适性提出了挑战——这类模型认为，物种形成连续体上的基因组差异积累始于受选择基因座的初始分化，随后通过连锁效应在相邻基因座间逐步扩散。