Islands promote diversification of the silvereye species complex: a phylogenomic analysis of a great speciator

Geographic isolation plays a pivotal role in speciation by restricting gene flow between populations through distance or physical barriers. However, the speciation process is complex, influenced by the interplay between dispersal ability and geographic isolation, as seen in "great speciators" - bird species that simultaneously have broad island distributions but high levels of subspecific diversity. Comparing genomic population differentiation in species that occupy both continental and island settings can reveal the effects of different forms of geographic isolation and validate if the mechanism proposed to catalyse a great speciator pattern, that is dispersal reduction following island colonisation, has occurred. The silvereye (Zosterops lateralis) counts with 16 subspecies (11 occurring on islands), distributed on the Australian continent and numerous southwest Pacific islands. We compared continental and island patterns of divergence using whole genome and morphological data. Australian mainland populations showed low genetic population structure and morphological diagnosability, suggesting the species' dispersal propensity in a continental setting is sufficient to overcome multiple forms of geographic barriers and large geographic distances. In contrast, most island populations were highly genomically structured with clearer morphological diagnosability even if separated by relatively short geographic distances. The inferred reduction of dispersal propensity in island situations is consistent with the proposed model of great speciator formation. Our phylogenomic analyses revealed both concordance and discrepancies between morphological subspecies classifications and genomic data. Our findings illustrate how genomic and morphological patterns across different geographic contexts can help reveal when specific speciation stages, such as great speciators, are likely to emerge.

地理隔离通过距离或物理屏障限制种群间的基因流，在物种形成过程中发挥关键作用。然而，物种形成过程极为复杂，受扩散能力与地理隔离之间相互作用的影响，正如“顶级成种类群（great speciators）”所展现的那样——这类鸟类类群同时具备广泛的岛屿分布范围与极高的亚种多样性。对同时栖息于大陆与岛屿生境的物种开展种群基因组分化比较，可揭示不同类型地理隔离的作用效应，并验证驱动顶级成种类群模式的核心机制——即岛屿定居后扩散能力降低——是否成立。银绣眼鸟（Zosterops lateralis）共计16个亚种（其中11个分布于岛屿），其分布范围涵盖澳大利亚大陆以及西南太平洋的众多岛屿。本研究利用全基因组与形态学数据，对比了该物种大陆与岛屿种群的分化模式。结果显示，澳大利亚大陆种群表现出较低的遗传种群结构与形态辨识度，表明该物种在大陆生境中的扩散倾向足以克服多种地理屏障与较大的地理距离。与之形成鲜明对比的是，多数岛屿种群即便地理间隔相对较短，也呈现出高度的基因组结构分化，且形态辨识度更高。所推断出的岛屿生境中扩散倾向降低的现象，与顶级成种类群形成的假说模型相符。本研究的系统基因组学分析结果显示，形态学亚种分类与基因组数据之间既存在一致性，也存在冲突。本研究结果阐明了不同地理背景下的基因组与形态学模式，如何助力揭示特定成种阶段（如顶级成种类群）的出现时机。