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

Alex Buerkle,Mark S Hibbins,Matthew W Hahn

doi:10.1371/journal.pgen.1009892

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.

Highlights

Introgression—the historical hybridization and subsequent backcrossing of previously isolated lineages—has come to the forefront of phylogenomics with the availability of genome sequencing
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

Summary

Introduction

Introgression—the historical hybridization and subsequent backcrossing of previously isolated lineages—has come to the forefront of phylogenomics with the availability of genome sequencing (reviewed in [1,2]). Investigating the effects of introgressed ancestry on quantitative trait evolution remains a challenge, despite recent theoretical and methodological advances [9–11]. This is because many processes besides introgression can shape the distribution of any particular character, including incomplete lineage sorting and convergence. Introgressed variants acting on gene expression either in cis or in trans may affect the evolution of gene expression across the genome. This could have potentially deleterious effects on fitness, which would be consistent with previous evidence for widespread selection against introgressed alleles [15–18]

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Conclusion