Local and temporal adaptation to climatic change in a wild tomato species via selective sweeps.

Positive Darwinian selection is the driving force underpinning local (in space) and temporal (in time) adaptation, and leaves footprints of selective sweeps at the underlying major genes. These two adaptive processes are classically considered independently, so that most genomic selection scans uncover only recent sweeps underpinning spatial adaptation. However, understanding if these adaptive processes are intermingled and share common genetic bases is crucial to predict a species evolutionary potential, for example in response to changing environmental conditions. We use whole genome data from six populations across three different habitats of the wild tomato species Solanum chilense, to 1) infer the past demographic history, and 2) search for genes under strong positive selection. We then correlate the demographic history, allele frequencies in space and time, the age of selection events and the reconstructed historical ecological distribution of the species over five main climatic periods spanning 150,000 years. We find evidence for several selective sweeps targeting regulatory networks involved in root hair development in low altitude, and response to photoperiod and vernalization in high altitude populations. These sweeps occur in a concerted fashion in a given regulatory gene network and only at particular time periods, thereby underpinning temporal local adaptation. These genes under positive selection provide subsequently the basis for spatial local adaptation to novel habitats when new ecological niches become available. Our results reveal the importance of jointly studying spatial and temporal adaptations in species during habitat colonization.