Species-specific loss of genetic diversity and inbreeding following agricultural intensification

Abstract

Land-use change from agricultural intensification is a major driver of global insect declines. We investigated the genetic consequences of grassland decline in Sweden by sequencing museum and modern specimens of three focal and five additional Polyommatinae butterfly species. From 59 historical and 90 contemporary genomes, we find a 6% decline in genetic diversity and increased isolation and inbreeding in the grassland specialist Cyaniris semiargus over the past 70 years. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus maintained genetic diversity and connectivity. Although currently genomic erosion is mild, we infer it lags considerably larger declines in effective population sizes. Using simulations, we demonstrate that only a small portion of genetic diversity is lost in early stages of decline, creating a genetic extinction debt. Two of five additional species show similar reductions, underscoring that restoration of grassland habitat is necessary to restore gene flow and halt further genomic erosion in grassland insects.