Data from: Evolutionary history of endemic Sulawesi squirrels constructed from UCEs and mitogenomes sequenced from museum specimens

Background: The Indonesian island of Sulawesi has a complex geological history. It is composed of several landmasses that have arrived at a near modern configuration only in the past few million years. It is the largest island in the biodiversity hotspot of Wallacea—an area demarcated by the biogeographic breaks between Wallace's and Lydekker's lines. The mammal fauna of Sulawesi is transitional between Asian and Australian faunas. Sulawesi's three genera of squirrels, all endemic (subfamily Nannosciurinae: Hyosciurus, Rubrisciurus and Prosciurillus), are of Asian origin and have evolved a variety of phenotypes that allow a range of ecological niche specializations. Here we present a molecular phylogeny of this radiation using data from museum specimens. High throughput sequencing technology was used to generate whole mitochondrial genomes (mitogenomes) and a panel of nuclear Ultra Conserved Elements (UCEs) providing a large genome-wide dataset for inferring phylogenetic relationships. Results: Our analysis confirmed monophyly of the Sulawesi taxa with deep divergences between the three endemic genera, which predate the amalgamation of the current island of Sulawesi. This suggests lineages may have evolved in allopatry after crossing Wallace's line. Nuclear and mitochondrial analyses were largely congruent and well supported, except for the placement of Prosciurillus murinus. Mitochondrial analysis revealed paraphyly for Prosciurillus, with P. murinus between or outside of Hyosciurus and Rubrisciurus, separate from other species of Prosciurillus. A deep but monophyletic history for the four included species of Prosciurillus was recovered with the nuclear data. Conclusions: The divergence of the Sulawesi squirrels from their closest relatives dated to ~9.7-12.5 million years ago (MYA), pushing back the age estimate of this ancient adaptive radiation prior to the formation of the current conformation of Sulawesi. Generic level diversification took place around 9.7 MYA, opening the possibility that the genera represent allopatric lineages that evolved in isolation in an ancient proto-Sulawesian archipelago. Incongruence between phylogenies based on nuclear and mitochondrial sequences could result from an ancient introgression event involving the smallest species Prosciurillus murinus and an unsampled lineage. Lineages have sorted for a long period of time after the mitochondrial introgression, resulting in negligible contribution to the nuclear genome in P. murinus.

背景：印度尼西亚苏拉威西岛地质历史复杂，由多个陆块拼接而成，直至数百万年前才形成接近现代的地理格局。它是华莱士区（Wallacea）生物多样性热点区域的最大岛屿——该区域以华莱士线与莱德克线之间的生物地理分界划定。苏拉威西岛的哺乳动物区系兼具亚洲与澳洲区系的过渡特征。苏拉威西岛的三个松鼠属均为特有属，隶属于倭松鼠亚科（Nannosciurinae）：鼠鼩松鼠属（Hyosciurus）、红松鼠属（Rubrisciurus）和前松鼠属（Prosciurillus），它们起源于亚洲，并演化出多样的表型以适应不同的生态位特化需求。本研究利用馆藏标本数据，构建了该类群的分子系统发育树。我们采用高通量测序技术，获取了完整线粒体基因组（mitogenomes）以及一组核超保守元件（Ultra Conserved Elements, UCEs）数据，由此获得了大规模的全基因组数据集，用于推断系统发育关系。
结果：本研究的分析证实，苏拉威西岛的松鼠类群为单系群，且三个特有属之间存在深度分化事件，其分化时间早于当前苏拉威西岛的拼接形成过程。这表明，这些类群在跨越华莱士线后，可能经历了异域分化演化。核基因与线粒体基因的分析结果整体一致且支持度良好，但前松鼠属（Prosciurillus murinus）的系统发育位置除外。线粒体分析显示前松鼠属为并系群：P. murinus位于鼠鼩松鼠属与红松鼠属之间或之外，与其他前松鼠属物种相互分离。而核基因数据则显示，本次研究纳入的四种前松鼠属物种构成一个深度分化但单系的类群。
结论：苏拉威西松鼠与其近缘类群的分化时间可追溯至约970万至1250万年前（million years ago, MYA），将这一古老适应辐射的时间节点提前至当前苏拉威西岛地理格局形成之前。属级别的分化发生在约970万年前，这表明各属可能是在古老的原苏拉威西群岛中孤立演化的异域类群。核基因与线粒体序列构建的系统发育树之间的不一致性，可能源于一场涉及最小体型物种——灰背前松鼠（Prosciurillus murinus）与未采样类群的古老基因渐渗事件。在线粒体渐渗发生后，类群经历了长期的谱系分选，使得P. murinus的核基因组中几乎未保留该渐渗事件的信号。