Genomics of incipient speciation in a highly vagile marine mammal: genome-wide analysis of demographic history, population structure and local adaptation in the endangered Galápagos sea lion

在查尔斯·达尔文的开创性著作《物种起源》出版150年后，野生动物形成物种的机制仍未得到解决。然而，基因组革命现在为我们提供了必要的工具来研究物种形成的基因组结构。在最有希望揭示控制适应和控制物种形成早期步骤的进化过程的系统中，沿着强环境梯度分化的进化年轻谱系。特别是，海洋物种提供了理想的系统，用于测试在缺乏基因流动物理障碍的情况下，生态分化选择是否会导致异质基因组分化。加拉帕戈斯海狮（Zalophus wollebaeki）就提供了这样一个系统，它占据了一个偏远、贫瘠的环境，自查尔斯·达尔文时代以来，这里一直是物种形成研究的沃土。这个物种在100多万年前从它的加利福尼亚姐妹（加利福尼亚扎洛菲斯）中分离出来，从那以后一直保持孤立。相对于物种的扩散能力，它的分布范围很小，但它的特点是在西部年轻岛屿周围营养丰富的土地和群岛中央浅层大陆架上的岛屿之间有一个陡峭的环境梯度。一项利用22颗微卫星和线粒体DNA进行的初步研究证明，这些环境差异转化为形态、饮食和潜在遗传学的显著差异。这挑战了基因流动的地理障碍是遗传分化所必需的观点，也使加拉帕戈斯海狮成为研究微进化过程的主要候选者，这些微进化过程在面对不受限制的扩散潜力时促进了局部适应和局部遗传分化。我们的提议将是第一个在野外独特的生态环境中利用后基因组时代的可能性。我们建议在整个物种范围内进行基因组规模的种群遗传分析，使用密切相关的南极海狗基因组作为参考。由此产生的数据将使我们能够确定生态早期物种形成的主要机制，识别物种形成岛（即携带不同选择特征的候选基因组区域），并将它们与不同的环境参数联系起来。这些数据也将提供一个理想的机会来测试理论预测，即性染色体比基因组的其余部分更快地形成物种。在这种独特的环境中，基因组规模的群体遗传方法和聚结模型的结合将产生对自然群体适应和物种形成的进化过程的基本见解。

One hundred and fifty years after Charles Darwins seminal work On the Origin of Species, the mechanisms by which animals speciate in the wild are still unresolved. However, the genomic revolution is now providing us with the necessary tools to investigate the genomic architecture of speciation. Among the most promising systems to reveal the evolutionary processes that control adaptation and govern the early steps of speciation are evolutionary young lineages diverging along strong environmental gradients. In particular, marine species provide ideal systems in which to test whether ecologically divergent selection in the absence of physical barriers to gene flow can lead to heterogeneous genomic divergence.The Galapagos sea lion (Zalophus wollebaeki) provides just such a system, occupying a remote, depauperate environment that has been a fertile ground for speciation research ever since the time of Charles Darwin. This species diverged from its Californian sister (Zalophus californianus) over one million years ago and has remained isolated ever since. Its range is tiny relative to the dispersal capability of the species but is characterized by a steep environmental cline between the nutrient rich grounds around the young western islands and the islands on the shallow central shelf of the archipelago. These environmental contrasts translate into marked differences in morphology, diet and the underlying genetics, as documented in a pilot study using 22 microsatellites and mitochondrial DNA. This challenges the view that geographic barriers to gene flow are required for genetic divergence and also makes the Galapagos sea lion a prime candidate for examining micro evolutionary processes that have facilitated local adaptation and localized genetic differentiation in the face of unrestricted dispersal potential.Our proposal will be among the first to harness the possibilities of the post genomic era in a unique ecological setting in the wild. We propose conducting genome-scale population genetic analyses across the entire species range, using the closely related Antarctic fur seal genome as a reference. The resulting data will allow us determine the primary mechanism underlying ecological incipient speciation, to identify speciation islands (i.e. candidate genomic regions carrying signatures of divergent selection) and to link these to divergent environmental parameters. These data will also provide an ideal opportunity to test the theoretical predication that the sex chromosomes speciate faster than the remainder of the genome. The combination of genome-scale population genetic approaches and coalescent modeling in this unique setting will yield fundamental insights into the evolutionary processes governing adaption and speciation in natural populations.