Demography, adaptation, and mating system shifts in the perennial plant Arabis alpina

Plants with an Arctic-alpine distribution are challenged by extreme temperatures, low water availability and short favorable seasons, and can be used as models to study adaptation to harsh environments. Furthermore, these species experience habitat loss and fragmentation due to climate change, and studying their evolution and genomic diversity can reveal possible responses to a warming climate. We study plant adaptation to harsh environments using the perennial, Arctic-alpine plant Arabis alpina as a model. Using population genomic approaches on a new, large-scale collection of 1161 individual plants of A. alpina, we reconstructed the ancient spread of this plant across Europe, which dates back 0.5 to 1 Million years ago (ya). Due to this ancient history, the species accumulated tremendous genetic divergence among regions and populations. In the present interglacial period, since the last glacial maximum (about 20,000 ya), we detect a widespread decline of diversity within populations, and increasing rates of drift, likely driven by warming temperatures. Across the range, we find signatures of selection associated with genes related to drought responses, with climatic variables such as aridity indexes, and with large genomic structural variants. Our results suggest that A. alpina has been struggling with increasing temperatures since the last glacial maximum, however with some potential for adaptation mediated by standing genetic variation that is present in local, isolated populations in a fragmented landscape. During its expansion across Europe, A. alpina evolved variable mating strategies ranging from obligate outcrossing, to mixed-mating, to selfing. Using genetic and genomic approaches, we find evidence for multiple independent transitions from outcrossing to selfing, mediated by transposable elements insertions, high-impact mutations, and structural variants at the self-incompatibility locus. Overall, our results suggest that A. alpina can serve as a model to understand species responses to climate change, and to understand the evolutionary and genomic consequences of variable mating strategies.