Genomic studies of isolation, diversity loss, and inbreeding in grassland butterflies

Land use change from agricultural intensification has been highlighted as one of the major drivers of global declines in insects, reducing species diversity and abundance and shifting community composition towards generalist species. However, it remains a challenge to determine how land use change impacts the genetic diversity of species and populations even if this diversity is vital to their long-term persistence. Reductions in genetic diversity are expected to reduce adaptive potential and increase the frequency of deleterious mutations, potentially reinforcing demographic declines. In this thesis, I investigate to what extent grassland habitat loss associated with agricultural intensification in southern Sweden has resulted in genetic diversity declines in grassland butterflies, and what genomic metrics best capture these declines. Utilizing genomic data across multiple species, I infer if differential demographic decline in generalists and specialists is reflected in patterns of genetic erosion. Through a spatial comparison of populations of three grassland butterfly species, I uncover that specialist species show stronger genetic structure, with one specialist species experiencing sufficient isolation to lead to higher rates of recent inbreeding compared to the other species. Associating genetic diversity with land cover variables, I find that genetic diversity is lower in populations with less grassland area in the surrounding landscape due to higher rates of inbreeding. Comparisons between contemporary samples and museum specimens of these same three species reveal that genetic diversity has declined over the past century, and that the genetic structure and inbreeding in the specialist species has arisen recently. Importantly, inbreeding has increased homozygosity of putative weakly deleterious mutations in this species, which may depress fitness of inbred individuals and reinforce decline. To determine if these patterns are general, I estimated the extent of genetic differentiation, reductions in effective population size, and recent inbreeding in Sweden’s most common grassland butterflies compared to the European Grassland Butterfly Indicator species. While estimates of heterozygosity varied by species, rates of inbreeding were distinctly higher in specialists, as were levels of genetic differentiation between localities. Trajectories of contemporary effective population size over time reveal that while many widespread species maintain high effective population sizes, specialists have dropped to sizes below 500 and even 50 over the past 30-50 years. Estimations of recent inbreeding and contemporary population size thus provide valuable indicators of genetic decline and should be evaluated in conservation assessments to incorporate information on reduced viability from genetic erosion. To make the methods used to perform such assessments more accessible I develop an automated bioinformatic pipeline for the analyses performed in this thesis, that I describe and provide as a resource. Together, my findings highlight that land use change has reduced functional connectivity and increased inbreeding in specialist grassland butterflies, and conservation efforts targeting habitat restorations that restore gene flow are necessary for the persistence of specialist grassland insect species.