Complex histories of gene flow and a mitochondrial capture event in a non-sister pair of bird

Hybridization, introgression, and reciprocal gene flow during speciation, specifically the generation of mitonuclear discordance, are increasingly observed as parts of the speciation process. Genomic approaches provide insight into where, when, and how adaptation operates during and after speciation and can measure historical and modern introgression. Whether adaptive or neutral in origin, hybridization can cause mitonuclear discordance by placing the mitochondrial genome of one species (or population) in the nuclear background of another species. The latter, introgressed species may eventually have its own mtDNA replaced or “captured” by other species across its entire geographical range. Intermediate stages in the capture process should be observable. Two non-sister species of Australasian monarch-flycatchers, Spectacled Monarch (Symposiachrus trivirgatus) mostly of Australia and Indonesia and Spot-winged Monarch (S. guttula) of New Guinea, present an opportunity to observe this process. We analysed thousands of single nucleotide polymorphisms (SNPs) derived from ultraconserved elements of all subspecies of both species. Mitochondrial DNA sequences of Australian populations of S. trivirgatus form two paraphyletic clades, one being sister to and presumably introgressed by S. guttula despite little nuclear signal of introgression. Population genetic analyses (e.g., tests for modern and historical gene flow and selection) support at least one historical gene flow event between S. guttula and Australian S. trivirgatus. We also uncovered introgression from Maluku island subspecies of S. trivirgatus into an island population of S. guttula, resulting in apparent nuclear paraphyly. We find that neutral demographic processes, not adaptive introgression, are the most likely cause of these complex population histories. We suggest that a Pleistocene extinction of S. guttula from mainland Australia resulted from range expansion by S. trivirgatus.

Methods
The data was collected using sequenced of ulraconserved element (UCE) target capture, and processed for a variety of population genetic and phylogenetic analyses. We also analyzed "bycatch" mitogenomes and previously sequenced mitochondrial genes..

物种形成过程中的杂交、基因渐渗与双向基因流，尤其是核质冲突（mitonuclear discordance）的产生，正越来越多地被视为物种形成过程的组成部分。基因组学方法可揭示适应性演化在物种形成过程中及之后的发生时间、空间位置与作用模式，还能量化历史和现代的基因渐渗事件。无论起源于适应性演化还是中性过程，杂交都可通过将一个物种（或种群）的线粒体基因组置于另一物种的核基因组背景中，引发核质冲突。后者，即发生渐渗的物种，最终可能在其整个地理分布范围内自身的线粒体DNA（mtDNA）被其他物种替换或“捕获”。该捕获过程的中间阶段应可被观测到。
两种非姊妹群的澳大拉西亚王鹟：主要分布于澳大利亚和印度尼西亚的斑眼王鹟（Spectacled Monarch, Symposiachrus trivirgatus）以及新几内亚的斑翅王鹟（Spot-winged Monarch, S. guttula），为观测该过程提供了理想研究体系。本研究对两个物种所有亚种的超保守元件（ultraconserved elements, UCEs）来源的数千个单核苷酸多态性（single nucleotide polymorphisms, SNPs）进行了分析。澳大利亚种群的S. trivirgatus线粒体DNA序列形成两个并系类群，其中一个类群与S. guttula互为姊妹群，且尽管核基因组中几乎没有渐渗信号，但推测其发生了来自S. guttula的基因渐渗。种群遗传学分析（例如现代与历史基因流检测及选择压力检验）支持S. guttula与澳大利亚种群S. trivirgatus之间至少发生过一次历史基因流事件。本研究还发现了来自S. trivirgatus马鲁古群岛亚种向S. guttula一个岛屿种群的基因渐渗事件，该事件导致了显著的核基因组并系性。本研究发现，中性种群动态过程而非适应性渐渗，是造成这些复杂种群演化历史的最可能原因。本研究推测，澳大利亚大陆的S. guttula在更新世的灭绝事件，是由S. trivirgatus的分布范围扩张所导致的。

研究方法
本研究通过超保守元件靶向捕获测序技术收集数据，并针对多种种群遗传学及系统发育分析进行了数据处理。此外，本研究还分析了"附带捕获"的线粒体基因组以及已发表的线粒体基因序列。