Cities as evolutionary incubators for the global spread of the Spotted Lanternfly

Abstract

Habitat destruction and invasive species pose two of the greatest global threats to biodiversity. These factors do not operate in isolation, and nowhere is their interaction more apparent than in urban environments. Urban organisms rapidly evolve under novel ecological circumstances where they also encounter anthropogenic opportunities for range expansion. Here, we examine the role of urbanization in the invasive success of an emerging global pest, the Spotted Lanternfly, during colonization and expansion. We demonstrate that the invasive population in the United States has undergone three sequential bottlenecks, resulting in significantly reduced genetic diversity and elevated inbreeding. The success of this invasive population may be in part attributable to adaptation in the native range prior to the invasion: we detect divergence between urban and rural lanternflies in Shanghai, China, (the invasion origin) in genes related to stress response, metabolism, and detoxification pathways. Additionally, we detect genomic signatures of selection in the invasive population suggesting adaptive refinement as the invasion progresses. This study provides evidence of adaptive evolution in response to urbanization despite substantial loss of genetic diversity, and implicates adaptive responses to pesticide application, dietary shifts, and climate in the invasive success of the Spotted Lanternfly.