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

Land-use change driven by agricultural intensification is a major contributor to insect declines globally. As a result of population decline and subdivision, species lose genetic diversity, reducing adaptive potential and increasing genetic load. We examine how genetic diversity has changed over the past century in three focal and five additional Polyommatinae butterfly species in Sweden by sequencing specimens from museum collections. Based on 59 historical and 90 contemporary genomes, we document a 6% decline in heterozygosity in the grassland specialist Cyaniris semiargus, driven by division into small, isolated populations. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus have maintained genetic diversity and connectivity. Reduced heterozygosity in Cy. semiargus reflects increases in runs of homozygosity, increasing the homozygosity of derived mutations at missense and conserved positions. While genomic erosion is currently relatively mild, it is expected to lag demographic change. We infer that demographic decline in Cy. semiargus is considerably larger than declines in genetic diversity to date. We use simulations to demonstrate that only mild losses of genetic diversity are expected at the early stages of demographic decline, leaving populations with substantial genetic extinction debt. We detect similar reductions in genetic diversity in two of five additional species, underscoring the need for restoring habitat connectivity and gene flow to limit further genomic erosion in specialist grassland insects. This study illustrates how incorporation of genetic monitoring into conservation planning can identify where demographic decline has left populations with a genetic extinction debt even after they stabilize.