Nonadaptive processes in primate and human evolution

Evolutionary biology has tended to focus on adaptive evolution by positive selection as the primum mobile of evolutionary trajectories in species while underestimating the importance of nonadaptive evolutionary processes. In this review, I describe evidence that suggests that primate and human evolution has been strongly influenced by nonadaptive processes, particularly random genetic drift and mutation. This is evidenced by three fundamental effects: a relative relaxation of selective constraints (i.e., purifying selection), a relative increase in the fixation of slightly deleterious mutations, and a general reduction in the efficacy of positive selection. These effects are observed in protein-coding, regulatory regions, and in gene expression data, as well as in an augmentation of fixation of large-scale mutations, including duplicated genes, mobile genetic elements, and nuclear mitochondrial DNA. The evidence suggests a general population-level explanation such as a reduction in effective population size (N(e)). This would have tipped the balance between the evolutionary forces of natural selection and random genetic drift toward genetic drift for variants having small selective effects. After describing these proximate effects, I describe the potential consequences of these effects for primate and human evolution. For example, an increase in the fixation of slightly deleterious mutations could potentially have led to an increase in the fixation rate of compensatory mutations that act to suppress the effects of slightly deleterious substitutions. The potential consequences of compensatory evolution for the evolution of novel gene functions and in potentially confounding the detection of positively selected genes are explored. The consequences of the passive accumulation of large-scale genomic mutations by genetic drift are unclear, though evidence suggests that new gene copies as well as insertions of transposable elements into genes can potentially lead to adaptive phenotypes. Finally, because a decrease in selective constraint at the genetic level is expected to have effects at the morphological level, I review studies that compare rates of morphological change in various mammalian and island populations where N(e) is reduced. Furthermore, I discuss evidence that suggests that craniofacial morphology in the Homo lineage has shifted from an evolutionary rate constrained by purifying selection toward a neutral evolutionary rate.