Population Genomics Reveals Small-Scale Metapopulation Structure of Two Strictly Aquatic Keystone Species in a Recently Restored Urban River System (Emscher, Germany)

Urbanization and the resulting modifications of freshwater ecosystems can play an important role in shaping metapopulation structure and dynamics of aquatic organisms. Ecological restoration aims at improving river ecosystems by reducing or removing anthropogenic stressors and habitat fragmentation, facilitating natural dispersal among population patches. However, the success of such ecological restoration measures is not guaranteed, and for many of the functionally important but smaller organisms, improved connectivity is difficult to assess. Here, genetic markers can help in assessing small-scale connectivity and in identifying persisting gene flow barriers. In this study used high-resolution genetic markers to study the metapopulation structure of two ecologically important amphipod species, Gammarus pulex and Gammarus fossarum, in the heavily urbanized Emscher catchment in Germany. This catchment was strongly degraded and polluted for over a century but has been restored over the past two decades. For both strictly aquatic species, we analyzed mitochondrial cytochrome c oxidase I (COI) gene sequences as well as nuclear genome-wide single nucleotide polymorphism (SNP) data. We detected strong metapopulation structure within both species, which was mainly driven by catchment affiliation, wastewater, large in-stream barriers, and recent recolonization of restored stream sections. However, population structure was not fully explained by these factors, indicating that eco-evolutionary factors such as priority effects, adaptation, or biotic interactions play a role in shaping the population structure. Furthermore, our data show a strong mito-nuclear discordance for both species with regard to detailed population structure and also the presence of possible cryptic species for G. pulex. Here, nuclear data indicate that the diverging mitochondrial lineages of G. pulex (Gp-C and Gp-E) represent only one species in this region. Our study shows how genetic markers can support the assessment of population connectivity and thus evaluate the success of ecological restoration.