Developmental Selection and the Perception of Mutation Bias

Abstract

The notion that mutations are random relative to their fitness effects is central to the Neo-Darwinian view of evolution. However, a recent interpretation of the patterns of mutation accumulation in the genome of Arabidopsis thaliana has challenged this notion, arguing for the presence of a targeted DNA repair mechanism that causes a nonrandom association of mutation rates and fitness effects. Specifically, this mechanism was suggested to cause a reduction in the rates of mutations on essential genes, thus lowering the rates of deleterious mutations. Central to this argument were attempts to rule out selection at the population level. Here, we offer an alternative and parsimonious interpretation of the patterns of mutation accumulation previously attributed to mutation bias, showing how they can instead or additionally be caused by developmental selection, that is selection occurring at the cellular level during the development of a multicellular organism. Thus, the depletion of deleterious mutations in A. thaliana may indeed be the result of a selective process, rather than a bias in mutation. More broadly, our work highlights the importance of considering development in the interpretation of population-genetic analyses of multicellular organisms, and it emphasizes that efforts to identify mechanisms involved in mutational biases should explicitly account for developmental selection.