Demographic modelling reveals a history of divergence with gene flow for a glacially tied stonefly in a changing post-Pleistocene landscape

Aim: Climate warming is causing extensive loss of glaciers in mountainous regions, yet our understanding of how glacial recession influences evolutionary processes and genetic diversity is limited. Linking genetic structure with the influences shaping it can improve understanding of how species respond to environmental change. Here, we used genome-scale data and demographic modelling to resolve the evolutionary history of Lednia tumana, a rare, aquatic insect endemic to alpine streams. We also employed a range of widely used data filtering approaches to quantify how they influenced population structure results. Location: Alpine streams in the Rocky Mountains of Glacier National Park, Montana, USA. Taxon: Lednia tumana, a stonefly (Order Plecoptera) in the family Nemouridae. Methods: We generated single nucleotide polymorphism data through restriction-site associated DNA sequencing to assess contemporary patterns of genetic structure for 11 L. tumana populations. Using identified clusters, we assessed demographic history through model selection and parameter estimation in a coalescent framework. During population structure analyses, we filtered our data to assess the influence of singletons, missing data and total number of markers on results. Results: Contemporary patterns of population structure indicate that L. tumana exhibits a pattern of isolation-by-distance among populations within three genetic clusters that align with geography. Mean pairwise genetic differentiation (F-ST) among populations was 0.033. Coalescent-based demographic modelling supported divergence with gene flow among genetic clusters since the end of the Pleistocene (similar to 13-17 kya), likely reflecting the south-to-north recession of ice sheets that accumulated during the Wisconsin glaciation. Main conclusions: We identified a link between glacial retreat, evolutionary history and patterns of genetic diversity for a range-restricted stonefly imperiled by climate change. This finding included a history of divergence with gene flow, an unexpected conclusion for a mountaintop species. Beyond L. tumana, this study demonstrates the complexity of assessing genetic structure for weakly differentiated species, shows the degree to which rare alleles and missing data may influence results, and highlights the usefulness of genome-scale data to extend population genetic inquiry in non-model species.