Urbanization affects population connectivity, reproductive success and phenotypic traits in the Mediterranean cliff species Brassica incana (Brassicaceae)

Biotic and abiotic changes induced by urbanization can highly affect the ecology and evolution of plant species. Indeed, urban development can have a major impact on plant population genomics, reproductive success and phenotypic traits hence influencing the adaptive strategies and the ecological functions of plant species within ecosystems. Through a holistic study of the impact of urbanization on the genetic and ecological dynamics of a Mediterranean plant species, we shed light on the mechanisms driving plant responses to urban environments. By focusing on 15 populations of the Mediterranean cliff species Brassica incana distributed along an urbanization gradient, we first analyzed the potential drivers of among-population genomic differentiation using a landscape genomics approach. Then, we provided a comprehensive understanding of the complex interplay among ecological factors (climate, herbivore damage, pollinator community), reproductive (relative fruit set and seed-ovule ratio) and phenotypic (glucosinolate content, flower number) traits involved in the response of B. incana populations to urban pressures using complementary Structural Equation Modeling (SEM) and correlative approaches. Our results show that urbanization reduces among-population connectivity by influencing the genomic differentiation among populations. Also, according to SEM analysis, urbanization showed direct and indirect (mediated by mean annual temperature) effects on both pollinator community and herbivory levels, and direct and indirect (mediated by honeybees and long-tongued bees) effects on plant reproductive success. Additionally, urban populations showed higher contents of a glucosinolate compound (glucobrassicin). Taken together, our findings suggest that urbanization can shape genomic differentiation, reproductive success and phenotypic variation. We showed that the impact of urbanization is rather complex and is likely mediated by the interplay between direct and indirect effects of abiotic and biotic conditions on B. incana. Overall, we documented how urban development can shape eco-evolutionary dynamics of a cliff species located in a densely inhabited Mediterranean area.