Rate of molecular evolution and pleiotropy on the evolutionary trajectories of penguin genes

Abstract Genes that participate in multiple biological processes through the proteins they encode can experience mutations that alter more than one of these functions. This potential for pleiotropic changes is known to modify the proportion of mutations that reach fixation, i.e., the molecular evolutionary rate of the gene. Simulations and empirical evidence suggest a negative correlation between the pleiotropic level of a gene and its rate of evolution. Nonetheless, this relation has not been studied under realistic settings that include the temporal and environmental context under which lineages and genomes evolve. Using Fisher’s geometric model (FGM), we demonstrate that this relationship develops over time, transitioning through three phases characterized by distinct signs and magnitudes of the pleiotropic effect, and that the onset of the pleiotropic effect depends on the initial fitness of the population. Analysis of over 8,000 genes from 15 penguin species reveals a robust concordance with theoretical predictions. Our findings exemplify how the increasing availability of high-resolution genomic datasets has significantly enhanced our ability to test evolutionary hypotheses raised by theoretical models.