Population Genomics of the "Arcanum" Species Group in Wild Tomatoes: Evidence for Separate Origins of Two Self-Compatible Lineages

Given their diverse mating systems and recent divergence, wild tomatoes ( section ) have become an attractive model system to study ecological divergence, the build-up of reproductive barriers, and the causes and consequences of the breakdown of self-incompatibility. Here we report on a lesser-studied group of species known as the "Arcanum" group, comprising the nominal species , , and . The latter two taxa are self-compatible but are thought to self-fertilize at different rates, given their distinct manifestations of the morphological "selfing syndrome." Based on experimental crossings and transcriptome sequencing of a total of 39 different genotypes from as many accessions representing each species' geographic range, we provide compelling evidence for deep genealogical divisions within ; only the self-incompatible lineage known as "var. marañón" has close genealogical ties to the two self-compatible species. Moreover, there is evidence under multiple inference schemes for different geographic subsets of var. marañón being closest to and , respectively. To broadly characterize the population-genomic consequences of these recent mating-system transitions and their associated speciation events, we fit demographic models indicating strong reductions in effective population size, congruent with reduced nucleotide and -locus diversity in the two independently derived self-compatible species.