Traditional phylogenetic models fail to account for variations in the effective population size

Abstract

A substitution represents the emergence and fixation of an allele in a population or species and is the fundamental event from which phylogenetic models of sequence evolution are devised. As a result of the increasing availability of genomic sequences, we can currently leverage interspecific variability while reconstructing the tree of life. Substitutions can thus more realistically be modeled as the product of mutation, selection, and genetic drift. However, it remains unclear whether this additional complexity affects our measures of evolutionary times and rates. This study seeks to answer this question by contrasting the traditional substitution model with a population genetic counterpart by using data from 4385 individuals distributed across 179 populations and representing 17 species of animals, plants, and fungi. We found that when the population genetics dynamic is modeled via the substitution rates, the evolutionary times and rates measured by these models are well correlated, suggesting that the substitution models are able to capture the time and pace of their population counterpart. However, a closer inspection of this result showed that the traditional models largely ignore the effect of population size, even when explicitly accounted for in the substitution rates, while the effects of mutation and selection are well captured. Our results indicate that superimposing population-genetics results on the substitution rates may be efficiently used to study mutation and selection biases, while other data sources (e.g., life history traits or polymorphisms) need to be additionally integrated to infer variations in the population size. We expect our results to help develop mutation-selection phylogenetic models and inspire unified frameworks between large and short evolutionary time scales.