Spatial proximity determines post-speciation introgression in Solanum

ABSTRACT An increasing number of phylogenomic studies have documented a clear ‘footprint’ of post-speciation introgression among closely-related species. Nonetheless, systematic genome-wide studies of factors influencing the likelihood of introgression remain rare. Here, we use an a priori hypothesis-testing framework, and introgression statistics, to evaluate the prevalence and frequency of introgression. Specifically, with whole genome sequences from 32 lineages of wild tomato species, we assess the effect of three factors on introgression: genetic relatedness, geographical proximity, and mating system differences. Using multiple trios within the ‘ABBA-BABA’ test, we find that one of our factors, geographic proximity, is consistently associated with evidence for recent introgression between species. Of 14 species pairs with ‘proximate’ versus ‘distant’ population comparisons, 12 showed evidence of introgression; in ten of these cases, this was more prevalent between geographically-closer populations. We found no evidence that introgression varies systematically with increasing genetic divergence between lineages or with mating system differences, although we have limited power to address the latter effect. While our analysis indicates that recent post-speciation introgression is frequent in this group, estimated levels of genetic exchange are modest (0.05-1.5% of the genome), so the relative importance of hybridization in shaping the evolutionary trajectories of these species could be limited. Regardless, similar clade-wide analyses of genomic introgression would be valuable for disentangling the major ecological, reproductive, and historical determinants of post-speciation gene flow, and for assessing the relative importance of introgression as a source of evolutionary change. IMPACT STATEMENT The formation of new species is traditionally viewed as a tree-like branching process, in which species are discrete branches that no longer share an ongoing genealogical connection with other, equally discrete, species. Recently this view has been challenged by numerous studies examining genealogical patterns across entire genomes (all the DNA of an organism); these studies suggest that the exchange of genes between different species (known as ‘introgression’) is much more common than previously appreciated. This unexpected observation raises questions about which conditions are most important in determining whether species continue to exchange genes after they diverge. Factors such as physical proximity, differences in reproductive mechanisms, and time since species shared a common ancestor, might all contribute to determining the prevalence of introgression. But to evaluate the general importance of these factors requires more than individual cases; many species comparisons, that differ systematically in one or more of these conditions, are needed. Here we use whole-genome information from 32 lineages to evaluate patterns of introgression among multiple species in a single, closely related group—the wild tomatoes of south America. We contrast these patterns among pairs of lineages that differ in their geographical proximity, reproductive system, and time since common ancestry, to assess the individual influence of each condition on the prevalence of introgression. We find that only one of our factors—geographical proximity—is consistently associated with greater evidence for recent introgression, indicating that this is largely shaped by the geographical opportunity for hybridization, rather than other plausible biological processes. Our study is one of the first to systematically assess the influence of general ecological and evolutionary conditions on the frequency of post-speciation introgression. It also provides a straightforward, generalizable, hypothesis-testing framework for similar systematic analyses of introgression in groups of other organisms in the future.