The effects of introgression across thousands of quantitative traits revealed by gene expression in wild tomatoes

Abstract

It is now understood that introgression can serve as powerful evolutionary force, providing genetic variation that can shape the course of trait evolution. Introgression also induces a shared evolutionary history that is not captured by the species phylogeny, potentially complicating evolutionary analyses that use a species tree. Such analyses are often carried out on gene expression data across species, where the measurement of thousands of trait values allows for powerful inferences while controlling for shared phylogeny. Here, we present a Brownian motion model for quantitative trait evolution under the multispecies network coalescent framework, demonstrating that introgression can generate apparently convergent patterns of evolution when averaged across thousands of quantitative traits. We test our theoretical predictions using whole-transcriptome expression data from ovules in the wild tomato genus Solanum. Examining two sub-clades that both have evidence for post-speciation introgression, but that differ substantially in its magnitude, we find patterns of evolution that are consistent with histories of introgression in both the sign and magnitude of ovule gene expression. Additionally, in the sub-clade with a higher rate of introgression, we observe a correlation between local gene tree topology and expression similarity, implicating a role for introgressed cis-regulatory variation in generating these broad-scale patterns. Our results reveal a general role for introgression in shaping patterns of variation across many thousands of quantitative traits, and provide a framework for testing for these effects using simple model-informed predictions. Author summary It is now known from studying large genetic datasets that species often hybridize and cross with each other over many generations – a phenomenon known as introgression. Introgression introduces new genetic variation into a population, and this variation can cause traits to be shared among the introgressing species. When researchers study the evolution of trait variation among species, this source of trait sharing is rarely accounted for. Here, we present a statistical model of the effects of introgression on trait variation. This model predicts that, when averaged across many thousands of traits, introgressing species are consistently more similar than expected from standard approaches. Researchers studying gene expression often consider the expression of many thousands of genes, making this a case where the expected effects of introgression are likely to manifest. We tested our model prediction using ovule gene expression data from the wild tomato genus Solanum, in two groups of species with evidence of historical introgression. We found that patterns of expression similarity in both groups are consistent with their histories of introgression and the predictions from our model. Our results highlight the importance of accounting for introgression as a source of trait variation among species.