Spatial sorting promotes rapid (mal)adaptation in the red-shouldered soapberry bug after hurricane-driven local...

Predicting future evolutionary change is a critical challenge in the Anthropocene as geographic range shifts and local extinction emerge as hallmarks of planetary change. Hence, spatial sorting-a driver of rapid evolution in which dispersal-associated traits accumulate along expanding range edges and within recolonized habitats-might be of growing importance in ecology and conservation. We report on the results of a natural experiment that monitored recolonization of host plants by the seed-feeding, red-shouldered soapberry bug, Jadera haematoloma, after local extinctions from catastrophic flooding in an extreme hurricane. We tested the contribution of spatial sorting to generate rapid and persistent evolution in dispersal traits, as well as in feeding traits unrelated to dispersal. Long-winged dispersal forms accumulated in recolonized habitats and due to genetic correlation, mouthparts also became longer and this shift persisted across generations. Those longer mouthparts were probably adaptive on one host plant species but maladaptive on two others based on matching the optimum depth of seeds within their host fruits. Moreover, spatial sorting eroded recently evolved adaptive divergence in mouthpart length among all host-associated biotypes, an outcome pointing to profound practical consequences of the extreme weather event for local adaptation, population resilience and evolutionary futures.