Phylogenomic comparative methods: Accurate evolutionary inferences in the presence of gene tree discordance

Phylogenetic comparative methods have long been a mainstay of evolutionary biology, allowing for the study of trait evolution across species while accounting for their common ancestry. These analyses typically assume a single, bifurcating phylogenetic tree describing the shared history among species. However, modern phylogenomic analyses have shown that genomes are often composed of mosaic histories that can disagree both with the species tree and with each other-so- called discordant gene trees. These gene trees describe shared histories that are not captured by the species tree, and therefore that are unaccounted for in classic comparative approaches. The application of standard comparative methods to species histories containing discordance leads to incorrect inferences about the timing, direction, and rate of evolution. Here, we develop two approaches for incorporating gene tree histories into comparative methods: one that constructs an updated phylogenetic variance-covariance matrix from gene trees, and another that applies Felsenstein's pruning algorithm over a set of gene trees to calculate trait histories and likelihoods. Using simulation, we demonstrate that our approaches generate much more accurate estimates of tree- wide rates of trait evolution than standard methods. We apply our methods to two clades of the wild tomato genus Solanum with varying rates of discordance, demonstrating the contribution of gene tree discordance to variation in a set of floral traits. Our approaches have the potential to be applied to a broad range of classic inference problems in phylogenetics, including ancestral state reconstruction and the inference of lineage- specific rate shifts.

Automated summary

Phylogenetic comparative methods are crucial in evolutionary biology, but they often fail to account for discordant gene trees that do not align with the species tree. We introduce two new methods that incorporate gene tree histories into comparative analysis and show that they provide more accurate estimates of trait evolution than traditional methods. Applying these methods to floral traits in the Solanum genus, we demonstrate the impact of gene tree discordance on trait variation. Our approaches have broad applications in phylogenetics, including ancestral state reconstruction and lineage-specific rate shifts.