Genomic signatures of rapid local selection and introgression drive adaptive phylogeography in the European river skater

Cycle of glacial contraction and postglacial expansion in widespread European organisms, as inferred from neutral genetic markers, has led to classic phylogeographic divergence and a primarily latitudinal gradient in genetic diversity. However, the relative contribution of adaptive loci, compared to neutral loci, in shaping complex phylogeographic patterns remains poorly understood. We generated extensive genomic datasets for the widespread European species Aquarius najas and its relatives (Aquarius cinereus and Aquarius ventralis), sampled across their entire European distribution. Our results revealed that A. najas is divided into northern and southern lineages, driven in part by major biogeographical barriers in Europe through neutral processes. Additionally, we discovered northern populations exhibiting unexpectedly high genetic diversity, consistent with the cryptic extra-Mediterranean refugia hypothesis. These populations showed evidence of strong, rapid local adaptation, as indicated by the identification of 52 temperature-associated genes (e.g., regulating MAPK thermosensitivity). For the Ibero-Maghrebian populations, our analyses uncovered significant mitochondrial and nuclear introgression from A. cinereus into A. najas. Notably, we identified adaptive introgressed genes, including an ATP-binding cassette (ABC) transporter and the zinc finger protein ZFP91, which likely enhance survival and fitness in the Maghreb region. Our study presents a comprehensive paradigm for understanding how widespread, limited-dispersal European species adapt to heterogeneous environments through the combined effects of rapid local selection and adaptive introgression, extending beyond the influence of neutral processes alone. Furthermore, we designed and implemented an extended framework for phylogeographic investigation that incorporates both neutral and adaptive dimensions.