Abstract

Simple SummaryIt is of great interest to quantify adaptive evolution in human lineage by studying genes under positive selection, since these genes could reveal insights into our own adaptive evolutionary history compared to our closely related species and often these genes are functionally important. We used the great apes as the subjects to detect gene-level adaptive evolution signals in all the great ape lineages and investigated the evolutionary patterns and functional relevance of these adaptive evolution signals. Even the differences in population size among these closely related great apes have resulted in differences in their ability to remove deleterious alleles and to adapt to changing environments, we found that they experienced comparable numbers of positive selection. Notably, we identified several genes that offer insights into great ape and human evolution. For example, SOD1, a gene associated with aging in humans, experienced positive selection in the common ancestor of the great ape and this positive selection may contribute to the aging evolution in great apes. Overall, an updated list of positively selected genes reported by this study not only informs us of adaptive evolution during great ape evolution, but is also helpful to the further study of non-human primate models for disease and other fields.Alleles that cause advantageous phenotypes with positive selection contribute to adaptive evolution. Investigations of positive selection in protein-coding genes rely on the accuracy of orthology, models, the quality of assemblies, and alignment. Here, based on the latest genome assemblies and gene annotations, we present a comparative analysis on positive selection in four great ape species and identify 211 high-confidence positively selected genes (PSGs). Even the differences in population size among these closely related great apes have resulted in differences in their ability to remove deleterious alleles and to adapt to changing environments, we found that they experienced comparable numbers of positive selection. We also uncovered that more than half of multigene families exhibited signals of positive selection, suggesting that imbalanced positive selection resulted in the functional divergence of duplicates. Moreover, at the expression level, although positive selection led to a more non-uniform pattern across tissues, the correlation between positive selection and expression patterns is diverse. Overall, this updated list of PSGs is of great significance for the further study of the phenotypic evolution in great apes.

Highlights

  • Adaptive evolution has been reported to be associated with many phenotypic changes in humans [1,2,3]

  • We observed that the majority (63%) of the positively selected genes (PSGs) are from multiple-gene families, suggesting various positive selection resulted in the functional divergence of duplicates. Based on these PSGs, we investigated their functional contribution to great ape evolution and their expression pattern

  • This study provides a timely update of PSG candidates that might have contributed to the adaptive evolution of great apes

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Summary

Introduction

Adaptive evolution has been reported to be associated with many phenotypic changes in humans [1,2,3]. Bakewell and colleagues [13] used this improved branch-site model to identify PSGs in the human and the chimpanzee, with rhesus as the outgroup They performed analysis based on old, less-complete genome assemblies without filtering for the low confidence PSG candidates, which will cause potential false negatives. Lee et al [14] performed the latest genome-scale positive selection test in primates to identify high-confidence PSGs with a stringent threshold. Their analysis was based on the site model, which cannot detect the branch-level positive selection signals [15], and they did not use the latest upgraded genome assemblies [16]

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