Drivers of avian genomic change revealed by evolutionary rate decomposition

Abstract

Modern bird diversity spans a striking array of forms, behaviours, and ecological roles. Analyses of molecular evolutionary rates can reveal the links between genomic and phenotypic change, but disentangling the drivers of rate variation has been difficult across large numbers of whole-genomes. Using comprehensive estimates of traits and evolutionary rates across a family-level phylogeny of birds, we show that clutch size, generation length, and beak shape are dominant predictors of genome-wide mutation rates. To identify the major axes of evolutionary rate variation, we employ covariance matrix eigendecomposition from rates estimated for branches of the avian phylogeny and across genomic loci. We find that the majority of rate variation occurs along the terminal branches of the phylogeny associated with extant families of birds. Additionally, we use principal components analyses to show that several axes of variation are linked with rapid evolution in microchromosomes immediately after the Cretaceous-Palaeogene transition. These apparent pulses of evolution are consistent with major changes in evolutionary rates in the machineries for meiosis, heart performance, and RNA splicing, surveillance, and translation. They also correlate with the diversification of ecological niches reflected in increased tarsus length. Collectively, our analyses paint a nuanced picture of avian evolutionary rates through time, revealing that the ancestors of the most diverse lineages of birds underwent major genomic changes related to mutation, gene usage, and niche expansion near the beginning of the Palaeogene period.