RecPD: A Recombination-Aware Measure of Phylogenetic Diversity

Abstract

A critical step in studying biological features (e.g., genetic variants, gene families, metabolic capabilities, or taxa) underlying traits or outcomes of interest is assessing their diversity and distribution. Accurate assessments of these patterns are essential for linking features to traits or outcomes and understanding their functional impact. Consequently, it is of crucial importance that the metrics employed for quantifying feature diversity can perform robustly under any evolutionary scenario. However, the standard metrics used for quantifying and comparing the distribution of features, such as prevalence, phylogenetic diversity, and related approaches, either do not take into consideration evolutionary history, or assume strictly vertical patterns of inheritance. Consequently, these approaches cannot accurately assess diversity for features that have undergone recombination or horizontal transfer. To address this issue, we have devised RecPD, a novel recombination-aware phylogenetic-diversity metric for measuring the distribution and diversity of features under all evolutionary scenarios. RecPD utilizes ancestral-state reconstruction to map the presence / absence of features onto ancestral nodes in a species tree, and then identifies potential recombination events in the evolutionary history of the feature. We also derive a number of related metrics from RecPD that can be used to assess and quantify evolutionary dynamics and correlation of feature evolutionary histories. We used simulation studies to show that RecPD reliably identifies evolutionary histories under diverse recombination and loss scenarios. We then apply RecPD in a real-world scenario in a preliminary study type III effector protein families secreted by the plant pathogenic bacterium Pseudomonas syringae and demonstrate that prevalence is an inadequate metric that obscures the potential impact of recombination. We believe RecPD will have broad utility for revealing and quantifying complex evolutionary processes for features at any biological level. AUTHOR SUMMARYPhylogenetic diversity is an important concept utilized in evolutionary ecology which has extensive applications in population genetics to help us understand how evolutionary processes have distributed genetic variation among individuals of a species, and how this impacts phenotypic diversification over time. However, existing approaches for studying phylogenetic diversity largely assume that the genetic features follow vertical inheritance, which is frequently violated in the case of microbial genomes due to horizontal transfer. To address this shortcoming, we present RecPD, a recombination-aware phylogenetic diversity metric, which incorporates ancestral state reconstruction to quantify the phylogenetic diversity of genetic features mapped onto a species phylogeny. Through simulation experiments we show that RecPD robustly reconstructs the evolutionary histories of features evolving under various scenarios of recombination and loss. When applied to a real-world example of type III secreted effector protein families from the plant pathogenic bacterium Pseudomonas syringae, RecPD reveals that horizontal transfer has played an important role in shaping the phylogenetic distributions of aa substantial proportion of families across the P. syringae species complex. Furthermore, we demonstrate that the traditional measures of feature prevalence are unsuitable as a metric for comparing feature diversity.