Return of the ghosts of dispersal past: historical spread and contemporary gene flow in the blue sea star Linckia laevigata

Marine animals inhabiting the Indian and Pacific oceans have some of the most extensive species ranges in the world, sometimes spanning over half the globe. These Indo-Pacific species present a challenge for study with both geographic scope and sampling density as limiting factors. Here, we augment and aggregate phylogeographic sampling of the iconic blue sea star, Linckia laevigata Linnaeus, 1758, and present one of the most geographically comprehensive genetic studies of any Indo-Pacific species to date, sequencing 392 base pairs of mitochondrial COI from 791 individuals from 38 locations spanning over 14,000 km. We first use a permutation based multiple-regression approach to simultaneously evaluate the relative influence of historical and contemporary gene flow together with putative barriers to dispersal. We then use a discrete diffusion model of phylogeography to infer the historical migration and colonization routes most likely used by L. laevigata across the Indo-Pacific. We show that estimates of genetic structure have a stronger correlation to geographic distances than to “oceanographic” distances from a biophysical model of larval dispersal, reminding us that population genetic estimates of gene flow and genetic structure are often shaped by historical processes. While the diffusion model was equivocal about the location of the mitochondrial most recent common ancestor (MRCA), we show that gene flow has generally proceeded in a step-wise manner across the Indian and Pacific oceans. We do not find support for previously described barriers at the Sunda Shelf and within Cenderwasih Bay. Rather, the strongest genetic disjunction is found to the east of Cenderwasih Bay along northern New Guinea. These results underscore the importance of comprehensive range-wide sampling in marine phylogeography.

栖息于印度洋与太平洋的海洋动物拥有全球最广的物种分布范围之一，部分类群的分布跨度甚至超过半个地球。这类印度-太平洋（Indo-Pacific）物种的研究面临两大限制因素：地理覆盖范围与采样密度。本研究对标志性物种蓝指海星（Linckia laevigata Linnaeus, 1758）的系统地理学采样工作进行了扩充与整合，目前已完成迄今针对印度-太平洋物种最全面的地理尺度遗传学研究之一：对覆盖14000余公里、38个采样点的791个个体的线粒体COI（mitochondrial COI）基因392个碱基对片段进行了测序。研究首先采用基于置换的多元回归方法，同步评估历史基因流、当代基因流以及潜在扩散障碍的相对影响程度。随后运用系统地理学的离散扩散模型，推断蓝指海星在印度-太平洋区域最可能的历史迁移与定殖路径。研究结果显示，遗传结构的估算结果与地理距离的相关性显著高于与幼虫扩散生物物理模型所得"海洋学距离"的相关性，这提示我们，基因流与遗传结构的群体遗传学估算往往受历史过程的塑造。尽管该扩散模型对线粒体最近共同祖先（mitochondrial most recent common ancestor, MRCA）的定位尚不明确，但研究表明基因流总体上以逐步扩散的方式在印度洋与太平洋间进行。本研究未支持此前提出的巽他陆架与森达瓦西湾（Cenderwasih Bay）内存在扩散障碍的结论，反而发现遗传分化最显著的区域位于新几内亚北部的森达瓦西湾东侧。这些研究结果凸显了在海洋系统地理学研究中开展全分布范围全面采样的重要性。