Rugged relief and climate promote isolation and divergence between two neotropical cold-associated birds

The role of historical factors in establishing patterns of diversity in tropical mountains has been of interest for some time. In these regions, the historical processes of range fragmentation and contraction followed by dispersal are thought to be mediated by the interplay between rugged relief and climate fluctuations and likely explain most of the dynamics of diversification in plants and animals. Although empirical studies addressing the interaction between climate and topography have provided invaluable insights into population divergence and speciation patterns in tropical montane organisms, a more detailed and robust test of such processes in an explicit spatio-temporal framework is still lacking. Consequently, our ability to gain insights into historical range shifts over time and the genomic footprint left by them is limited. Here we used niche modeling and subgenomic population-level datasets to explore the evolution of two species of warbling finches disjunctly distributed across the Montane Atlantic Forest, a Neotropical region with complex geological and environmental histories. Population structure inferences suggest a scenario of three genetically differentiated populations, which are congruent with both geography and phenotypic variation. Demographic simulations support asynchronous isolation of these populations as recently as ~40 kya, relatively stable population sizes over recent time, and past gene flow subsequent to divergence. Throughout the last 800 ky, niche models predicted extensive expansion into lowland areas with increasing overlap of species distributions during glacial periods, with prominent retractions and isolation into higher altitudes during interglacials, which are in line with signs of introgression of currently isolated populations. These results support a dual role of cyclical climatic changes: population divergence and persistence in mountain tops during warm periods followed by periods of expansion and admixture in lower elevations during cold periods. Shallow genetic divergence could be associated with undiscovered cryptic diversity in this global biodiversity hotspot.

长期以来，历史因素在塑造热带山地生物多样性格局中的作用，始终是学界关注的核心议题之一。在这类区域，分布区片段化、收缩后再发生扩散的历史过程，被认为由崎岖地形与气候波动的相互作用所介导，且该过程或可解释动植物物种多样化动态的多数成因。尽管针对气候与地形相互作用的实证研究，已为热带山地生物的种群分化与物种形成格局提供了极为宝贵的认知，但在明确的时空框架下对上述过程开展更细致且稳健的检验，目前仍属空白。因此，我们解析历史分布区随时间变迁的轨迹，以及这些变迁所留下的基因组印记的能力，仍受到诸多限制。本研究利用生态位模型（niche modeling）与亚基因组种群级数据集，对间断分布于山地大西洋森林（Montane Atlantic Forest）——一个地质与环境演化历史复杂的新热带区——的两种鸣雀的演化历程展开探究。种群结构推断结果显示存在三个遗传分化种群，该结果与地理分布格局及表型变异均保持一致。种群历史动态模拟结果支持这些种群的异步隔离事件最晚发生于约4万年前，且近期种群规模相对稳定，分化后曾存在过基因交流。在过去80万年中，生态位模型预测：冰期时期物种分布区会向低地大范围扩张，分布重叠程度随之升高；而间冰期时期则会显著收缩并隔离至更高海拔区域，这一结果与当前隔离种群间存在基因渐渗的证据相符。上述结果支持周期性气候变化的双重作用：暖期时种群发生分化并在山地山顶持续存续，冷期时则向低海拔区域扩张并发生基因混合。该全球生物多样性热点地区中较浅的遗传分化，或与尚未被发现的隐存多样性相关。