Species-specific loss of genetic diversity and exposure of deleterious mutations following agricultural intensification

Agriculture driven land-use change is a major contributor to insect declines globally. As a result of population decline and subdivision, species lose genetic diversity, potentially reducing adaptive potential and increasing genetic load, reinforcing decline. We examine how genetic diversity has changed over the past century in three Polyommatinae butterfly species in Sweden, leveraging genome sequencing of specimens from museum collections. Based on 59 historical and 90 contemporary genomes, we document a 6% decline in genetic diversity in the strongly grassland associated Cyaniris semiargus , driven by increased population isolation. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus have largely maintained genetic diversity and connectivity over the study period. The reduction in heterozygosity in Cy. semiargus results from increases in runs of homozygosity. Thus, loss of functional connectivity has led to inbreeding in Cy. semiargus , exposing greater proportions of weakly deleterious mutations and variants in highly conserved regions, in homozygous states. This realized burden likely reduces mean fitness and reinforces population decline, highlighting the need for well-connected grassland landscapes to maintain grassland specialist functional connectivity and genetic diversity. We complement these analyses with five additional Polyommatinae species, uncovering that warning- and alarm rates of decline are found in three of those, including in Cy. semiargus , currently listed as of least concern. This study highlights the necessity of incorporating genetic data into conservation planning, as threats from genetic erosion are not captured by census-based conservation assessments.