Speciation and adaptation in Antarctic sea spiders: Assessing the relative importance of genetic drift and natural selection using comparative population genomic and morphological approaches

对物种形成和适应过程的分析是理解生物多样性是如何产生以及如何应对不断变化的环境的基础。研究这种过程的理想生态系统是南大洋。南极洲周围寒冷的水域有丰富的、高度特有的底栖动物。最近的研究发现，这些物种中的许多是由一组离散的遗传支系组成的，这些遗传支系被解释为以前未被识别的物种，辐射于更新世。这些神秘的物种可以通过分子方法(例如DNA条形码)来区分，在某些情况下还可以通过细致的形态分析来区分。通常情况下，物种形成事件被解释为受最近冰川的驱动。假设物种形成是偶然发生的，因为以前的大量种群在冰川盛期被隔离到小型的异地避难所，在那里它们受到随机遗传漂移的强烈影响。由于以前分子技术的局限性，物种形成的替代模式很少被探索。来自其他生态系统的研究表明，生态物种形成，即由于强烈的差异选择而产生的分歧，是一种明显的替代模式。在这里，我们建议使用高分辨率的种群基因组方法，结合形态分析，在自然和非实验室环境中测试相互竞争的南大洋物种形成模型。作为一个测试案例，我们将研究南大洋一个特别成功的底栖物种群体的遗传漂移和选择模式：海蜘蛛(海蜘蛛纲)。在我们早期研究的基础上，我们将分析两个物种群体的中性和非中性标记的基因组模式：巨尾巨尾轮虫(Colossendeis Megalonix)和帕塔纳罗非鱼(Pallenopsis Pattonica)。这两个海蜘蛛物种复合体是解决这一提议目标的良好模式，因为它具有以下几个特点：1)存在许多遗传上不同的神秘物种，2)形态支持其中一些物种，3)它们广泛的分布范围，包括受过去冰川影响较小的南极大陆架和亚南极地区，4)它们流动性低。如果主要由冰川避难种群的遗传漂移驱动的异地物种形成是主要的进化力量，我们预计中性等位基因的随机固定和种群瓶颈的特征在受冰川严重影响的地区将是最高的。或者，如果自然选择一直是促进物种形成的中心进化力量，我们预计会在基因和表型水平上出现强烈的选择特征，特别是在共生关系(生态特征置换)方面。我们将研究整个基因组的变异，以评估随机变异与非随机变异。拟议的研究将在系统检验自然选择在南大洋进化中的相对重要性方面迈出重要的第一步。

The analysis of speciation and adaptation processes is fundamental to understand how biodiversity is generated and how it responds to changing environments. An ideal ecosystem to study such processes is the Southern Ocean. The cold waters around Antarctica host a rich and highly endemic benthic fauna. Recent studies have found that many of these species consist of groups of discrete genetic clades interpreted as previously unrecognized species that radiated in the Pleistocene. These cryptic species can be distinguished with molecular methods (e.g. DNA barcoding) and in some cases with meticulous morphological analyses. Typically the speciation events are interpreted as being driven by recent glaciations. The assumption is that speciation occurred by chance when formerly large populations were isolated into small allopatric refugia during glacial maxima, where they were then subjected to the strong effects of random genetic drift. Alternative models of speciation are rarely explored due to previous limitations in molecular techniques. Studies from other ecosystems suggest that ecological speciation, i.e., divergence due to strong differential selection, is one obvious alternative model. Here we propose to use high-resolution population genomic approaches coupled with morphological analyses to test competing Southern Ocean speciation models in a natural and non-laboratory setting. As a test case we will study patterns of genetic drift and selection in a particularly successful group of Southern Ocean benthic species: the sea spiders (Pycnogonida). Building on our earlier studies, we will analyse genomic patterns of neutral and non-neutral markers in two species flocks: Colossendeis megalonyx and Pallenopsis patagonica. These two sea spider species complexes are good models to address the objectives of this proposal because of several characteristics: 1) The presence of many genetically divergent cryptic species, 2) morphological support some of these species, 3) their broad distribution range including both Antarctic continental shelf and sub-Antarctic regions less affected by past glaciations, 4) their low mobility. If allopatric speciation driven largely by genetic drift in glacial refugial populations is the primary evolutionary force, we expect random fixation of neutral alleles and signatures of population bottlenecks to be highest in heavily ice-affected regions. Alternatively, if natural selection has been the central evolutionary force promoting speciation, we expect strong signatures of selection on geno- and phenotype level in particular in sympatry (ecological character displacement). We will investigate variation across whole genomes to assess random vs. non-random variation. The proposed study will make an important first step in systematically testing for the relative importance of natural selection in evolution in the Southern Ocean.