Nuclear phylogeography reveals strong impacts of gene flow in big brown bats

Aim: Understanding speciation mechanisms requires disentangling processes that promote and erode population-level divergence. Three hypotheses are raised that contemporary population structure is mainly shaped by refugial divergence, post-glacial gene flow, or combined effects of both. Testing these hypotheses requires range-wide phylogeography and integrative analyses across scales. Here we aim to 1) re-estimate the previously unresolved nuclear phylogeography of a widespread bat; 2) test the above three phylogeographic hypotheses; and 3) inform conservation management under climate change.

Location: North America including Caribbean.

Taxon: The big brown bat (Eptesicus fuscus).

Methods: We collected range-wide samples and genome-wide markers using restriction site-associated DNA sequencing. Population structure was analyzed by clustering methods and spatial estimations. Nuclear phylogeography was estimated using tree methods (concatenation and coalescent) and network analyses (TreeMix). Phylogeographic hypotheses were tested by comparing alternative evolutionary scenarios using demographic modeling. Species distribution modeling was used to help identify Pleistocene refugia and predict future range shifts under climate change.

Results: We identified three populations in the Caribbean, Eastern, and Western North America. The west population further split into three phylogeographic clades in Pacific, Southwestern North America, and Mexico. Discordances among mitochondrial and nuclear topologies reflected strong impacts of gene flow without sex biases. Demographic modeling supported scenarios of historical isolation followed by secondary gene flow and estimated Holocene divergence time. Species distribution was overall continuous during glaciation with possible regional isolation, and northward range shifts were predicted under future climate change.

Main Conclusions: Our results supported the hypothesis that combined effects of historical isolation and secondary gene flow shaped the contemporary population divergence. We showed that climate change probably triggered the initial divergence and that gene flow has strong impacts on the observed nuclear phylogeography. Our empirical study demonstrates dynamic within-species processes generating the population divergence that predates speciation.

研究目的：解析物种形成机制需要厘清促进与削弱种群水平分化（population-level divergence）的过程。目前提出3种假说，认为当代种群结构主要受避难所分化（refugial divergence）、冰期后基因流（post-glacial gene flow）或二者共同作用塑造。检验这些假说需要开展广域系统地理学（range-wide phylogeography）研究及多尺度整合分析。本研究旨在：1）重新解析此前尚未明确的广布蝙蝠的细胞核系统地理学格局；2）检验上述3项系统地理学假说；3）为气候变化背景下的保护管理提供科学依据。
研究区域：涵盖加勒比海地区的北美洲。
研究类群：大棕蝠（Eptesicus fuscus）。
研究方法：本研究采集了广域分布的样本，并利用限制性位点关联DNA测序（restriction site-associated DNA sequencing）获取全基因组分子标记。通过聚类分析方法与空间估测方法解析种群结构；采用系统发育树构建方法（联配法与溯祖法）及网络分析（TreeMix）估算细胞核系统地理学格局；通过比较不同演化场景的种群历史动态建模（demographic modeling）结果，对上述系统地理学假说进行检验；借助物种分布模型（species distribution modeling）识别更新世避难所（Pleistocene refugia）并预测气候变化情景下物种未来分布范围的变化。
研究结果：本研究在加勒比海、北美东部及北美西部共识别出3个种群；西部种群进一步划分为太平洋、北美西南部及墨西哥3个系统发育支系。线粒体与细胞核基因拓扑结构间的不一致性，反映出无性别偏向的基因流具有强烈影响。种群动态建模支持“历史隔离后发生二次基因流”的演化场景，并估算出全新世的分化时间。冰期期间物种分布整体呈连续状态，仅存在局部区域隔离；未来气候变化情景下预测物种分布范围将向北迁移。
主要结论：本研究结果支持“历史隔离与二次基因流共同作用塑造了当代种群分化”的假说。研究表明，气候变化或为初始种群分化的诱因，且基因流对观测到的细胞核系统地理格局具有显著影响。本实证研究揭示，种内动态演化过程可产生早于物种形成的种群分化。