Abstract

Rate of substitution of genomic regions is among the most debated intrinsic features that impact phylogenetic informativeness. However, this variable is also coupled with rates of nonsynonymous substitutions that underscore the nature and degree of selection on the selected genes. To empirically address these variables, we constructed four completely overlapping data sets of plastid matK, atpB, rbcL, and mitochondrial matR genes and used the rosid lineage (angiosperms) as a working platform. The genes differ in combinations of overall rates of nucleotide and amino acid substitutions. Tree robustness, homoplasy, accuracy in contrast to a reference tree, and phylogenetic informativeness are evaluated. The rapidly evolving/unconstrained matK faired best, whereas remaining genes varied in degrees of contribution to rosid phylogenetics across the lineage's 108 million years evolutionary history. Phylogenetic accuracy was low with the slowly evolving/unconstrained matR despite least amount of homoplasy. Third codon positions contributed the highest amount of parsimony informative sites, resolution and informativeness, but magnitude varied with gene mode of evolution. These findings are in clear contrast with the views that rapidly evolving regions and the 3rd codon position have inevitable negative impact on phylogenetic reconstruction at deep historic level due to accumulation of multiple hits and subsequent elevation in homoplasy and saturation. Relaxed evolutionary constraint in rapidly evolving genes distributes substitutions across codon positions, an evolutionary mode expected to reduce the frequency of multiple hits. These findings should be tested at deeper evolutionary histories.

Highlights

  • Genomic regions vary considerably in their potential phylogenetic informativeness and subsequent contribution to resolving a given set of taxa over specified time points

  • Our study demonstrates that tree robustness and phylogenetic informativeness for the four genes work in concert with their mode and tempo of evolution

  • The study underscores the need for assessments of phylogenetic informativeness of genomic regions for a given biological lineage within the framework of overall rates of nucleotide as well as nonsynonymous substitutions across their historic divergence

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Summary

Introduction

Genomic regions vary considerably in their potential phylogenetic informativeness and subsequent contribution to resolving a given set of taxa over specified time points. Among the properties inherent to genomic regions, rate of nucleotide substitution is regarded to have a profound impact in phylogenetic reconstruction [1,2,3,4,5,6,7,8]. The exclusion of rapidly evolving regions from deep phylogenetic reconstruction is generally based on the premise that multiple hits confounded by extended time scale could be significant enough to conceal phylogenetic signals and elevate homoplasy, with saturation reaching levels that can negatively impact tree structure [9,11,14,15]. Opposing points have been raised that promote the effectiveness of rapidly evolving and less constrained genomic regions in deep-level phylogenetics [2,13,23–

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