Population history shapes urban evolutionary dynamics: distinct genetic structure across urban and rural Europe in two lepidopterans

Urbanization is transforming environments globally. The altered abiotic conditions and biotic interactions in urban habitats impose divergent selection pressures on urban versus rural populations, while genetic drift may also be significant in typically small urban populations. A key question in urban evolution concerns the origin and spread of urban genotypes. Examples exist of both single and multiple origins of urban genotypes, but these have proven difficult to generalize. Here, we address genetic differentiation among urban populations, among rural populations, and between urban and rural populations. We conducted an extensive population genomic double digest restriction-site associated DNA sequencing analysis of two non-model grassland lepidopterans, Coenonympha pamphilus and Chiasmia clathrata, across Europe. The genetic population structures of the study species were strikingly different: Co. pamphilus showed strong population differentiation, while this was almost absent in Ch. clathrata, which instead showed signs of high current and past gene flow among populations. The results of Co. pamphilus are consistent with multiple origins of urban populations, and multiple origins also seem plausible in Ch. clathrata. These results suggest that past and large-scale population dynamics need to be integrated into urban evolution research, because population history affects urban evolutionary dynamics.