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.

大洋岛屿在进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，但过往研究几乎仅聚焦于陆地生物，对海洋物种的关注相对匮乏。本研究以加拉帕戈斯异齿鲨（*Heterodontus quoyi*）与单核苷酸多态性（single nucleotide polymorphisms, SNPs）为研究手段，探讨一种无幼体扩散能力的浅海海洋物种的进化过程，及其对遗传分化与岛屿生物地理学格局的影响。中央岛群逐步分离形成各独立岛屿的过程中，群岛间逐渐形成了不同水深的海水屏障，成为加拉帕戈斯异齿鲨扩散的阻碍。阻力隔离（Isolation-by-resistance）分析表明，海洋水深与历史海平面波动改变了种群间的遗传连通性。上述过程最终催生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，且二者随岛屿面积与地理隔离程度发生相应变化。本研究结果表明，岛屿形成与气候周期塑造了扩散能力受限的沿岸海洋生物的遗传分化与生物地理学格局，这一规律与陆地类群相一致。鉴于全球大洋岛屿均存在类似的生态情景，本研究为海洋进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的参考意义。