Data from: Range instability leads to cytonuclear discordance in a morphologically cryptic ground squirrel species complex

The processes responsible for cytonuclear discordance frequently remain unclear. Here, we employed an exon capture dataset and demographic methods to test hypotheses generated by species distribution models to examine how contrasting histories of range stability vs. fluctuation have caused cytonuclear concordance and discordance in ground squirrel lineages from the Otospermophilus beecheyi species complex. Previous studies in O. beecheyi revealed three morphologically cryptic and highly divergent mitochondrial DNA lineages (named the Northern, Central, and Southern lineages based on geography) with only the Northern lineage exhibiting concordant divergence for nuclear genes. Here, we showed that these mtDNA lineages likely formed in allopatry during the Pleistocene, but responded differentially to climatic changes that occurred since the last interglacial (~120,000 years ago). We find that the Northern lineage maintained a stable range throughout this period, correlating with genetic distinctiveness among all genetic markers and low migration rates with the other lineages. In contrast, our results suggested that the Southern lineage expanded from Baja California Sur during the Late Pleistocene to overlap and potentially swamp a contracting Central lineage. High rates of intraspecific gene flow between Southern lineage individuals among expansion origin and expansion edge populations largely eroded Central ancestry from autosomal markers. However, male-biased dispersal in this system preserved signals of this past hybridization and introgression event in matrilineal-biased X-chromosome and mtDNA markers. Our results highlight the importance of range stability in maintaining the persistence of phylogeographic lineages, whereas unstable range dynamics can increase the tendency for lineages to merge upon secondary contact.

核质不一致性（cytonuclear discordance）背后的形成机制往往尚未明确。据此，本研究依托外显子捕获数据集（exon capture dataset）与种群统计分析方法，检验由物种分布模型（species distribution models）推导得到的假说，以解析贝氏黄鼠（Otospermophilus beecheyi）物种复合体内地松鼠支系的分布区稳定与波动的差异化历史如何引发核质一致性（cytonuclear concordance）与核质不一致性的分化。
此前针对贝氏黄鼠的研究已发现3个形态隐存、分化程度极高的线粒体DNA（mtDNA, mitochondrial DNA）支系，按地理分布分别命名为北部支系、中部支系与南部支系，且仅北部支系的核基因（nuclear genes）表现出与线粒体分化一致的谱系分化。本研究显示，上述线粒体支系大概率形成于更新世的异域分化过程中，但在末次间冰期（约12万年前）以来的气候变迁中呈现出差异化的响应。其中北部支系在该时期内始终维持稳定的分布区，这与其所有遗传标记（genetic markers）下的遗传分化特征、与其余支系间较低的迁移率均呈显著相关。与之相反，本研究结果显示南部支系于更新世晚期从下加利福尼亚半岛南部发生扩张，其分布范围与正在收缩的中部支系发生重叠，并可能通过基因流淹没了中部支系的遗传组分。南部支系的扩张起源种群与扩张边缘种群间存在极高的种内基因流，这极大程度上清除了常染色体标记（autosomal markers）中保留的中部支系祖先遗传信号。但本研究体系中的雄性偏向扩散（male-biased dispersal），使得母系遗传偏好的X染色体与mtDNA标记中，仍保留了过往杂交与渐渗事件（hybridization and introgression event）的信号。本研究结果凸显了分布区稳定性在维持系统地理学支系（phylogeographic lineages）存续中的关键作用，而不稳定的分布区动态则会提升支系在二次接触（secondary contact）时发生融合的概率。