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

Abstract

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 (Lepidoptera: Lycaenidae) butterfly species in southern Sweden, leveraging genome sequencing of specimens from museum collections. Based on 63 historical and 92 contemporary genomes, we document a general decline in genetic diversity and reveal that the extent of decline depends on habitat specialization. The habitat generalist has retained most of its genetic diversity and connectivity. In contrast, the two specialists have declined sufficiently that even common variation is being eroded by drift, with up to a 3.3% reduction in heterozygosity per decade in the strongly grassland associatedCyaniris semiargus. While this sharp decline has reduced total genetic load in the two specialist species, increased population isolation has led to inbreeding inCy. semiargus, exposing a greater proportion of load in homozygous state. This realized load 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 data on seven additional Polyommatinae species, uncovering that declines are common across the group, with alarming rates of genetic decline in species listed as viable. This study highlights the urgency of incorporating genetic data into conservation planning, as threats from genetic erosion are not captured by current conservation assessment.