Ancient demographic reconstruction and spat temporal population genomics of European nightjar

The sequenced genomes in this project were used for two sub-projects, detailed below:Ancient Demographic Reconstruction:A species' demographic history provides important context to contemporary population genetics and insights into past responses to climate change. An individual's genome offers a view into the evolutionary history of current populations. Pairwise Sequentially Markovian Coalescent (PSMC) analysis uses information from a single genome to identify changes in effective population size over the last 5 million years. In this study, we applied PSMC analysis to two European nightjar (Caprimulgus europaeus) genomes, sampled from Northwest and Southern Europe, to explore the demographic history of nightjars in Europe. We successfully reconstructed the effective population size over the last 5 million years. Our analysis revealed that the effective population size of nightjars increased during stable warm periods and decreased during cooler spans and prolonged glacial periods, in response to global climate change. PSMC analysis on the pseudo-diploid combination of the two genomes showed fluctuations in gene flow between ancestral populations over time, with gene flow ceasing by the last-glacial period. Our results suggest possible divergence in the European nightjar population, with timings consistent with differentiation driven by isolation in different refugia during glaciation periods. Additionally, our findings indicate that migratory behavior in nightjars likely evolved before the last-glacial period and persisted throughout the Pleistocene. However, further genetic structure analysis of individuals from known breeding sites across the species' contemporary range is necessary to understand the extent and origins of range-wide differentiation in nightjars.Nightjar Spatio-temporal Population Genomics:Migratory birds are inherently mobile, a strategy that may reduce the impacts of habitat loss and fragmentation on genetic structuring and diversity. However, specialist resource requirements and distribution at range edges may counteract these benefits. The European nightjar (Caprimulgus europaeus) is a long-distance migratory bird and a habitat specialist. Like other long-distance migrants, nightjars have experienced a significant demographic decline across the British Isles and much of Northern and Western Europe over the last century. Despite the species' mobility, limited ringing recoveries suggest high site fidelity and little movement between breeding sites in the British Isles, the species' western range limit. With the population decline in nightjars well-documented in the British Isles, there is a need to quantify the extent and genetic impacts. We applied full genome resequencing to 60 historic (1841-1980) and 36 modern individual nightjars from the British population. Our results showed a statistically significant 34.8% loss in heterozygosity over the last ~180 years in this population, indicating a move away from panmixia and demonstrating weak spatial structure in the modern population. Such fine-scale structuring in migratory birds is rare. Our findings provide a case study on the impact of fragmentation on a species with specialist resource requirements at its range limit. Similar negative demographic trends in nightjars and other long-distance migrants in Northern and Western Europe suggest that the genetic signature found in the British population may be representative of other nightjar populations and European avifauna more broadly. While our results indicate no immediate cause for conservation concern for nightjars, they do show a trajectory of declining genetic diversity and increasing structure, potentially shared with other migratory species. Our study underscores the value of applying spatio-temporal population genetics analysis to migratory bird populations, despite their inherent mobility.

本项目所获得的测序基因组被应用于两项子研究，详情如下：

一、古人口统计学重建
物种种群的人口历史可为当代种群遗传学研究提供重要背景，并助力理解其过往对气候变化的响应。个体基因组能够展现当前种群的演化历程。成对序列马尔可夫溯祖（Pairwise Sequentially Markovian Coalescent, PSMC）分析可利用单个基因组的信息，识别近500万年内有效种群规模的变化。本研究对两份分别采自西北欧与南欧的欧洲夜鹰（European nightjar, *Caprimulgus europaeus*）基因组开展了PSMC分析，以探究欧洲地区夜鹰的种群人口历史。我们成功重建了近500万年内的有效种群规模。分析结果显示，欧洲夜鹰的有效种群规模在气候稳定温暖的时期扩张，而在凉爽时段与长期冰期阶段收缩，以响应全球气候变化。对两份基因组的伪二倍体组合开展的PSMC分析显示，祖先种群间的基因流随时间发生波动，并在末次冰期停止了基因交流。研究结果表明欧洲夜鹰种群可能存在分化，其分化时间与冰期阶段不同避难所隔离所驱动的分化时间相符。此外，研究结果还表明，夜鹰的迁徙行为可能在末次冰期之前就已演化形成，并在整个更新世（Pleistocene）中持续存在。不过，为明确欧洲夜鹰全分布范围种群分化的程度与起源，仍需对来自其当代分布范围内已知繁殖地的个体开展进一步的种群遗传结构分析。

二、夜鹰时空种群基因组学
候鸟天生具有移动性，这一策略或可减轻栖息地丧失与片段化对种群遗传结构及多样性的影响。然而，特化的资源需求与分布范围边缘的限制可能抵消这类益处。欧洲夜鹰（*Caprimulgus europaeus*）是长距离迁徙鸟类，同时也是栖息地特化物种。与其他长距离迁徙鸟类类似，在过去一个世纪中，欧洲夜鹰在不列颠群岛以及北欧与西欧的大部分区域都经历了显著的种群数量下降。尽管该物种具有移动性，但有限的环志回收数据表明，其具有较高的恋巢性，在不列颠群岛（该物种的西部分布极限）的繁殖地之间几乎没有移动。鉴于不列颠群岛的夜鹰种群下降已被充分记录，我们有必要量化其下降程度与遗传影响。我们对来自不列颠种群的60份历史样本（采集于1841-1980年）与36份现代个体样本开展了全基因组重测序。研究结果显示，在过去约180年间，该种群的杂合度（heterozygosity）显著下降了34.8%，表明其正偏离随机交配（panmixia），并展现出现代种群中微弱的空间结构。这类在候鸟中出现的精细尺度种群结构较为罕见。本研究结果为探究分布范围边缘的特化资源需求物种受栖息地片段化的影响提供了典型案例。北欧与西欧地区夜鹰及其他长距离迁徙鸟类出现的类似负向人口趋势表明，不列颠种群所呈现的遗传特征，或可代表其他夜鹰种群乃至更广泛的欧洲鸟类区系。尽管研究结果显示夜鹰暂无直接的保育关切，但它们确实呈现出遗传多样性下降与种群结构增强的趋势，这一趋势可能也存在于其他迁徙物种中。本研究强调了，尽管候鸟天生具有移动性，对其种群开展时空种群遗传学分析仍具有重要价值。