Selective sweeps linked to the colonization of novel habitats and climatic changes in a wild tomato species.

Positive selection is the driving force underpinning local adaptation and leaves footprints of selective sweeps on the underlying major genes. Quantifying the timing of selection and revealing the genetic bases of adaptation in plant species occurring in steep and varying environmental gradients are crucial to predict a species' ability to colonize new niches. We use whole-genome sequence data from six populations across three different habitats of the wild tomato species Solanum chilense to infer the past demographic history and search for genes under strong positive selection. We then correlate current and past climatic projections with the demographic history, allele frequencies, the age of selection events and distribution shifts. Several selective sweeps occur at regulatory networks involved in root-hair development in low altitude and response to photoperiod and vernalization in high-altitude populations. These sweeps appear to occur in a concerted fashion in a given regulatory gene network at particular periods of substantial climatic change. Using a unique combination of genome scans and modelling of past climatic data, we quantify the timing of selection at genes likely underpinning local adaptation to semiarid habitats.

Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats.

Nucleotide binding site, leucine-rich repeat receptors (NLRs) are canonical resistance (R) genes in plants, fungi and animals, functioning as central (helper) and peripheral (sensor) genes in a signalling network. We investigate NLR evolution during the colonization of novel habitats in a model tomato species, Solanum chilense. We used R-gene enrichment sequencing to obtain polymorphism data at NLRs of 140 plants sampled across 14 populations covering the whole species range. We inferred the past demographic history of habitat colonization by resequencing whole genomes from three S. chilense plants from three key populations and performing approximate Bayesian computation using data from the 14 populations. Using these parameters, we simulated the genetic differentiation statistics distribution expected under neutral NLR evolution and identified small subsets of outlier NLRs exhibiting signatures of selection across populations. NLRs under selection between habitats are more often helper genes, whereas those showing signatures of adaptation in single populations are more often sensor-NLRs. Thus, centrality in the NLR network does not constrain NLR evolvability, and new mutations in central genes in the network are key for R-gene adaptation during colonization of different habitats.