Parallel polygenic urban adaptation despite high gene flow in a coastal marine invertebrate

Abstract

Urbanization results in novel environments, offering a unique opportunity to investigate natural selection on small spatiotemporal scales. Although each city is different, geographically distinct cities can in some ways represent evolutionary replicates, allowing for the investigation of parallel and predictable evolutionary responses to urban environments. Additionally, there are few examples of urban adaptation in high gene flow marine systems, whose patterns might differ markedly from aquatic and terrestrial systems. Using whole genomes from Pacific purple sea urchins (Strongylocentrotus purpuratus) across three coastal cities spanning >2000km, we investigated genomic signals for adaptation to urban environments. We found genetic variants differentiating urban and nonurban sites within each city region, despite high gene flow and little evidence for differentiation across latitudinal gradients. While these SNP-level candidates for selection were largely non-overlapping, polygenic approaches uncover a distinct parallel signal of urban adaptation across the sampled range. Our results suggest that adaptation over small scale urbanization gradients is possible even in high gene flow systems and the polygenic architecture of adaptation is, at least in part, parallel. More broadly, our work highlights the importance of polygenic methods in ecological genomics in expanding our understanding of how evolutionary forces operate in natural systems.