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

查尔斯·达尔文在物种起源方面的开创性工作已经过去了150年，但动物在野外繁殖的机制仍然悬而未决。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。在揭示控制适应和控制物种形成早期步骤的进化过程方面，最有希望的系统之一是沿着强烈的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来测试在没有物理障碍的基因流动的情况下生态差异选择是否会导致异质基因组差异。加拉帕戈斯海狮(Zalophus Wollebaeki)就提供了这样的系统，占据了自查尔斯·达尔文时代以来一直是物种形成研究的肥沃土壤的偏远、贫瘠的环境。这个物种在100多万年前从它的加州姊妹(Zalophus Calfornianus)中分离出来，从那以后一直与世隔绝。与物种的扩散能力相比，它的范围很小，但其特点是在年轻的西部岛屿周围营养丰富的土地和群岛浅中央陆架上的岛屿之间有一个陡峭的环境斜坡。正如一项使用22个微卫星和线粒体DNA的初步研究所证明的那样，这些环境差异转化为形态、饮食和潜在遗传学上的显著差异。这挑战了这样一种观点，即基因流动的地理障碍是遗传分化所必需的，也使加拉帕戈斯海狮成为研究微观进化过程的主要候选者，这些过程促进了局部适应和局部遗传分化，面对不受限制的扩散潜力。我们的提议将是首批在野外独特的生态环境中利用后基因组时代的可能性的建议之一。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，以密切相关的南极毛海豹基因组为参考。由此产生的数据将使我们能够确定生态初始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)，并将这些与不同的环境参数联系起来。这些数据还将提供一个理想的机会，来检验性染色体比基因组的其余部分更快形成的理论预测。在这一独特的环境中，基因组规模的种群遗传方法和联合建模的结合将对管理自然种群适应和物种形成的进化过程产生基本的见解。

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.