DataSheet_1_Demographic Histories and Genome-Wide Patterns of Divergence in Incipient Species of Shorebirds.docx

Understanding how incipient species are maintained with gene flow is a fundamental question in evolutionary biology. Whole genome sequencing of multiple individuals holds great potential to illustrate patterns of genomic differentiation as well as the associated evolutionary histories. Kentish (Charadrius alexandrinus) and the white-faced (C. dealbatus) plovers, which differ in their phenotype, ecology and behavior, are two incipient species and parapatrically distributed in East Asia. Previous studies show evidence of genetic diversification with gene flow between the two plovers. Under this scenario, it is of great importance to explore the patterns of divergence at the genomic level and to determine whether specific regions are involved in reproductive isolation and local adaptation. Here we present the first population genomic analysis of the two incipient species based on the de novo Kentish plover reference genome and resequenced populations. We show that the two plover lineages are distinct in both nuclear and mitochondrial genomes. Using model-based coalescence analysis, we found that population sizes of Kentish plover increased whereas white-faced plovers declined during the Last Glaciation Period. Moreover, the two plovers diverged allopatrically, with gene flow occurring after secondary contact. This has resulted in low levels of genome-wide differentiation, although we found evidence of a few highly differentiated genomic regions in both the autosomes and the Z-chromosome. This study illustrates that incipient shorebird species with gene flow after secondary contact can exhibit discrete divergence at specific genomic regions and provides basis to further exploration on the genetic basis of relevant phenotypic traits.

解析存在基因流的初期物种（incipient species）如何维持种群，是进化生物学领域的核心科学问题之一。对多个个体开展全基因组测序（whole genome sequencing），可为解析基因组分化模式及相关演化历史提供重要契机。环颈鸻（Kentish plover，Charadrius alexandrinus）与白脸鸻（white-faced plover，C. dealbatus）在表型、生态与行为特征上均存在显著差异，二者为东亚地区邻域分布的初期物种。已有研究表明，这两种鸻之间存在伴随基因流的遗传分化。在此研究背景下，解析基因组水平的分化模式，并明确特定基因组区域是否参与生殖隔离与局部适应过程，具有重要科学价值。本研究基于从头组装（de novo）的环颈鸻参考基因组与重测序种群数据，首次对这两种初期物种开展种群基因组学（population genomics）分析。研究结果显示，两种鸻的谱系在核基因组与线粒体基因组中均存在显著分化。通过基于模型的溯祖分析（coalescence analysis），我们发现：在末次冰期（Last Glaciation Period），环颈鸻的种群规模呈扩张趋势，而白脸鸻的种群规模则发生衰退。此外，两种鸻最初以异域分化的方式形成，后续发生二次接触并伴随基因流。这一过程导致全基因组整体分化水平较低，但我们在常染色体（autosomes）与Z染色体（Z-chromosome）中均发现了少量高度分化的基因组区域。本研究证实，经历二次接触后仍存在基因流的初期滨鸟物种，可在特定基因组区域呈现显著分化；同时为后续探究相关表型性状的遗传基础提供了重要依据。