What Darwin couldn't see: Island formation and historical sea levels shape genetic divergence and island biogeography in a coastal marine species

Oceanic islands play a central role in the study of evolution and island biogeography. The Galapagos Islands are one of the most studied oceanic archipelagos but research has almost exclusively focused on terrestrial organisms compared to marine species. Here we used the Galapagos bullhead shark (Heterodontus quoyi) and single nucleotide polymorphisms (SNPs) to examine evolutionary processes and their consequences for genetic divergence and island biogeography in a shallow-water marine species without larval dispersal. The sequential separation of individual islands from a central island cluster gradually established different ocean depths between islands that pose barriers to dispersal in H. quoyi. Isolation-by-resistance analysis suggested that ocean bathymetry and historical sea level fluctuations modified genetic connectivity. These processes resulted in at least three genetic clusters that exhibit low genetic diversity and effective population sizes that scale with island size and the level of geographic isolation. Our results exemplify that island formation and climatic cycles shape genetic divergence and biogeography of coastal marine organisms with limited dispersal comparable to terrestrial taxa. Because similar scenarios exist in oceanic islands around the globe our research provides a new perspective on marine evolution and biogeography with implications for the conservation of island biodiversity.

大洋岛屿在演化生物学与岛屿生物地理学研究中具有核心地位。加拉帕戈斯群岛（Galapagos Islands）是全球研究最为深入的大洋群岛之一，但相较于海洋物种，过往相关研究几乎仅聚焦于陆生生物。本研究以加拉帕戈斯加平头鲨（Heterodontus quoyi）与单核苷酸多态性（single nucleotide polymorphisms, SNPs）为研究工具，针对一种不具备幼体扩散能力的浅海海洋物种，解析其演化过程及其对遗传分化与岛屿生物地理学格局的影响。中心岛屿群逐步依次分离形成各个独立岛屿，各岛屿间逐渐形成了不同水深，这些水深成为加平头鲨扩散的障碍。阻力隔离分析结果显示，海洋水深与历史海平面波动改变了种群的遗传连通性。上述过程最终形成了至少三个遗传聚类群，这些类群的遗传多样性与有效种群规模均较低，且其规模与岛屿面积及地理隔离程度呈正相关。本研究结果证实，岛屿形成与气候周期塑造了扩散能力有限的沿岸海洋生物的遗传分化与生物地理学格局，这一特征与陆生类群相似。鉴于全球范围内的大洋岛屿均存在类似的演化场景，本研究为海洋演化与生物地理学研究提供了全新视角，同时对岛屿生物多样性保护具有重要参考价值。