Phylogeographic pattern of range expansion provides evidence for cryptic species lineages in Silene nutans in Western Europe

As a result of recent or past evolutionary processes, a single species might consist of distinct Evolutionary Significant Units (ESUs), even corresponding to cryptic species. Determining the underlying mechanisms of range shifts and the processes at work in the build-up of divergent ESUs requires elucidating the factors that contribute to population genetic divergence across a species’ range. We investigated the large-scale patterns of genetic structure in the perennial herbaceous plant species Silene nutans (Caryophyllaceae) in Western Europe. We sampled and genotyped 111 populations using 13 nuclear microsatellite loci and 6 plastid single-nucleotide polymorphisms. Broad-scale spatial population genetic structure was examined using Bayesian clustering, spatial multivariate analyses and measures of hierarchical genetic differentiation. The genotypic structure of S. nutans was typical of a predominantly allogamous mating system. We also identified plastid lineages with no intra-population polymorphism, mirroring two genetically differentiated nuclear lineages. No evidence of admixture was found. Spatial trends in genetic diversity further suggested independent leading-edge expansion associated with founding events and subsequent genetic erosion. Overall, our findings suggested speciation processes in S. nutans and highlighted striking patterns of distinct stepwise recolonisation of Western Europe shaped by Quaternary climate oscillations. Two main potential ESUs can be defined in Western Europe, corresponding to Eastern and Western nuclear-plastid lineages. In situ preservation of populations and genetic rescue implying ex situ conservation techniques should take the lineage identity into account. This is particularly true in Great Britain, northern France and Belgium, where S. nutans is rare and where distinct lineages co-occur in close contact.

受新近或远古演化过程影响，单一物种可能包含多个独立的进化显著单元（Evolutionary Significant Units, ESUs），甚至可对应隐存物种。阐明物种分布范围扩张的内在机制，以及驱动分化型进化显著单元形成的过程，需要解析在物种整个分布区内导致种群遗传分化的各类因素。本研究针对西欧地区多年生草本植物垂花麦瓶草（Silene nutans，石竹科Caryophyllaceae）的种群遗传结构大尺度格局展开探究。我们通过13个核微卫星位点与6个质体单核苷酸多态性位点，对111个种群进行了采样与基因分型，并采用贝叶斯聚类、空间多变量分析以及层级化遗传分化测度等方法，对大尺度空间种群遗传结构进行了解析。垂花麦瓶草的基因型结构符合以异交为主的交配系统特征。研究还发现了无种群内多态性的质体谱系，其对应两个遗传分化显著的核谱系，且未检测到种群遗传混杂的迹象。遗传多样性的空间分布趋势进一步表明，存在与奠基事件及后续遗传侵蚀相关的独立前沿扩张过程。综合来看，本研究结果揭示了垂花麦瓶草的物种形成过程，并凸显出受第四纪气候波动驱动的西欧地区独特的阶段性逐步再定殖格局。在西欧地区可界定出两类主要的潜在进化显著单元，分别对应核-质体谱系的东部与西部分支。种群的原地保护以及需借助迁地保护技术的遗传拯救工作，均应考量谱系的身份特征。这一点在英国、法国北部与比利时地区尤为关键：这些区域内垂花麦瓶草种群较为稀少，且不同谱系近距离共存。