Gene Flow Disruption and Population Declines in a Soil Arthropod in Fragmented Habitats

The intensification of land use over past millennia has accelerated habitat loss and fragmentation. This is hypothesized to lead to reductions in population sizes and restrictions in gene flow, processes that amplify genetic drift with profound negative impacts on species and populations. However, empirical data on the population genetic impacts of habitat fragmentation remain limited, particularly for presumed abundant species such as insects. Reports of dramatic insect and arthropod declines are increasing, and their short generation times and limited dispersal capacities make them especially vulnerable to habitat fragmentation. To substantiate the hypothesis that habitat fragmentation negatively impacts genetic composition and demography, we combined historical agricultural land use data from Denmark with whole-genome resequencing of 25 populations of the collembolan Entomobrya nicoleti from natural grasslands. Abundance data indicate that agricultural expansion reduces habitat suitability and fragments populations. Demographic modelling shows that intensification of agricultural land use coincides with severe declines in effective population sizes. It is likely that these declines have yet to reach their full effect on current levels of genetic diversity because of the 'drift debt,' where the genetic diversity of recently declined populations will erode over future generations. Gene flow estimates revealed sharp recent declines that coincide with agricultural intensification. Our results underscore that even seemingly abundant species in fragmented landscapes can experience severe reductions in effective population size and gene flow. These demographic shifts predict future genetic erosion, highlighting the delayed yet inevitable consequences of habitat fragmentation for population persistence.