Past Environmental Change and Seasonal Migration Shaped Pronounced Variability in the Phylogenomic History of a Morphologically Cryptic Bird Radiation

Aim Modelling demographic changes through time in combination with phylogenomic reconstructions provides a promising avenue to better understand the impact of past environmental changes on biogeographic patterns, yet we have only begun to exploit this potential. Here, based on genome resequencing data, we studied how regionally contrasting environmental conditions and variation in seasonal migration behaviour and dispersal ability influenced diversification of a cryptic bird radiation containing evolutionary lineages with extensive variation in distribution ranges across Eurasia. Location Eurasia. Taxon Avian genus Riparia. Methods We analysed full genome data of 24 individuals including all Eurasian Riparia taxa using multi‐pronged phylogenomic and demographic analyses. Hand‐wing index (HWI) was used as a proxy for migration and dispersal behaviour. Results Collared R. riparia and pale sand martin R. diluta showed genomic divergence at inter‐ and intraspecific levels, aligning with described subspecies. The large Eurasian range of nominate R. r. riparia resulted from prolonged population growth during the Late Pleistocene rather than recent post‐glacial expansion as suggested earlier from mitochondrial DNA. Pronounced seasonal migration and dispersal propensity likely allowed the colonisation of a large range and impeded population differentiation. However, the divergence of southern R. r. shelleyi likely happened through a reduction in seasonal migration behaviour. The four evolutionary lineages of R. diluta showed independent demographic trajectories. After initial differentiation in contrasting environments, the evolution of distinct seasonal migration behaviour likely became crucial for maintaining genomic diversity. Conclusions Our comparative genomic analyses allowed us to pinpoint how regional variation in past environmental changes and life‐history traits led to contrasting evolutionary trajectories in a single bird radiation. This underpins the importance of such analyses across the tree of life to increase our understanding of the factors shaping species' demographic histories, not least for assessing their potential reaction to current human‐induced climate change.