Adaptation to seasonal drought in Arabis alpina is linked to the demographic history and climatic changes since the last glacial maximum

Abstract

Understanding how species adapt to new environments is a central goal in evolutionary biology, and a topical question in climate change research. Here, we sequenced the genomes of 426 individuals of the perennial, Arctic-alpine herb Arabis alpina to study demography and adaptation, with a focus on populations in Northern Spain, that experience warm and dry summers. Our inference supports a scenario in which A. alpina colonized Northern Spain in a range expansion event that started near the Alps around 216 thousand years ago (kya). During the last glacial episode (115 to 12 kya), this expansion proceeded Westward, and effective population sizes were large across Europe, likely due to a larger suitable habitat for A. alpina. These ancient demographic events gave rise to a highly diverged genetic lineage in Northern Spain. In the present interglacial (between 12 kya and present), populations became increasingly fragmented, and lost genetic diversity across Europe. Furthermore, we detected signatures of selection at genes associated with responses to abiotic stress, including drought stress, and regulation of growth, for instance at SC5D and NAC055, which reflects the climatic changes since the last glacial period. Notably, an ancient polymorphism at the gene FRL1 emerged as a candidate for conferring variation in flowering behavior, and for contributing to adaptation to drought. Our study suggests that the combination of ancestral variation in flowering behavior, and positive selection on new mutations involved in drought responses, underlies the evolution of a new trait syndrome, and adaptation to climate change.