Unravelling the determinants of the rate of adaptive evolution at the molecular level

Ever since Darwin presented natural selection as a driver of evolution, evolutionary biologists have thrived to understand how beneficial mutations shape species adaptation to their environment. Studying adaptation, however, requires an understanding of the complex dynamics between nucleotides, sequences, proteins, organisms, populations, and species. In other words, it requires assessing the interplay of evolutionary processes across systems. Here, I studied adaptation in such a way by exploring the frequency and nature of adaptive mutations within genes, within genomes, and between species. At the intramolecular level, this project revealed that the residue’s solvent accessibility acts as the primary determinant of rates of adaptive substitutions both in animals and in plants, where adaptive mutations are more frequent at the protein surface. These analyses further showed higher rates of adaptation for genes encoding proteins with central cellular functions, which are the ones usually targeted by pathogens during host infection. These findings, therefore, suggested that protein adaptive evolution proceeds through interactions between molecules, particularly at the interspecific level, where host-pathogen coevolution likely plays a central role. By taking a step back and looking at adaptation at different time-scales within the genome, this thesis revealed the role of young genes in adaptive evolution. As these genes are further away from their fitness optimum, these findings suggested that proteins adapt in an “adaptive walk” manner. This project further highlighted that the distribution of adaptive mutations across time follows a pattern of diminishing returns. Looking at an even broader scale by studying adaptation at the species level and considering the effect of intramolecular variation across several animal species, this thesis demonstrated a negative correlation between rates of adaptive substitutions and the effective population size (N_e). Despite the relatively weak signal, these findings contradict initial population genetics theory. Instead, they seem to agree with theoretical expectations at the phenotypic space. In turn, the results regarding negative selection confirm the N_e hypothesis, where the efficiency of selection is stronger in large-N_e species. This effect was well depicted in the differences of the distribution of fitness effects between buried and exposed residues, where the former accumulates comparatively more mild effect mutations in low-N_e species. This project further expanded our findings at the intramolecular level, by revealing the strong influence of the protein’s macromolecular structure on rates of molecular adaptation across several taxa. By assessing the interplay of adaptive mutations across distinct organizational levels, this thesis provided a more profound understanding of rates of adaptive evolution at the molecular level, thus delivering a comprehensive view of the molecular basis of adaptation.


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