Copy number variations shape genomic structural diversity underpinning ecological adaptation in the wild tomatoSolanum chilense

Abstract

AbstractCopy Number Variations (CNVs) are genomic structural variations constituting genetic diversity and underpinning rapid ecological adaptation. The timing and target genes of adaptation by means of CNVs are yet to be explored at the population level in the tomato clade. Therefore, we characterize the CNV landscape ofSolanum chilense, a wild tomato species, using whole-genome data of 35 individuals from seven populations. We identify 212,207 CNVs, including 160,926 deletions and 51,281 duplications. We find CNVs for both intergenic and coding regions, and a higher number of CNVs in recently diverged populations occupying more recently colonized habitats. Population structure analyses based on CNVs and single nucleotide polymorphisms are in agreement, highlighting that the distribution of CNVs is shaped by past demographic and colonization events. Furthermore, we identify 3,539 candidate genes with highly divergent copy number profiles across populations. These genes are functionally associated with response to abiotic stimuli and stress and linked to multiple pathways of flowering time regulation. Gene copy number variation exhibits two evolutionary trends: a contraction with gene loss in central and southern coast populations, and an expansion with gene gain in the southern highland group. Genome-environments association ultimately links the dynamics of gene copy number to six climatic variables and suggests that natural selection has likely shaped patterns of CNV in response to the climatic changes during the southward range expansion ofS. chilense. Our findings provide insights into the role of CNVs underlying ecological adaptation to recently colonized habitats.