Habitat fragmentation reshapes genomic footprints of selection in a forest herb

Abstract: Understanding the combined effects of climate change and habitat fragmentation on the adaptive potential of plant populations is essential for devising effective conservation strategies. This is particularly important where mating system variation impacts the evolutionary consequences of habitat fragmentation. Here we aimed to reveal how habitat fragmentation and climate adaptation jointly influence the evolutionary trajectories in Primula elatior, a heterostylous self-incompatible and dispersal-constrained forest herb. We quantified the genomic variation and degree of herkogamy, a floral trait reducing self-pollination, across 60 geographically paired populations of Primula elatior across Europe, each pair featuring contrasting levels of habitat fragmentation. Our findings revealed a large and unique set of adaptive outliers in more fragmented landscapes, compared to high-connectivity ones, despite the geographic proximity of the sampling pairs. This suggests elevated selective pressures in fragmented habitats, mirrored by a reduced adaptive potential to cope with climate change. Finally, a minority of genetic variants associated with herkogamy were influenced by current levels of habitat fragmentation and population size, potentially signalling early indicators of evolutionary mating system changes in response to pollinator limitation. Because evolutionary trajectories and adaptive potential are expected to be increasingly affected by habitat fragmentation, our findings underscore the importance of considering both habitat fragmentation and climate adaptation in conservation research and planning.