Nonadaptive Genetic Change in Human and Primate Evolution

Abstract

Abstract Evolutionary change can occur by nonadaptive processes, such as random genetic drift, and as a consequence of selection on linked genetic variants. In addition, if selective regimes change over time, an allele currently at a high frequency because of past fitness advantage may be suboptimal for its present environment. Small effective population size along the human lineage increased the influence of drift, rendering mutations with slight effects on fitness effectively neutral. Demographic events like spatial expansions and population bottlenecks shape most of the genetic variation within and among modern populations. Natural selection itself may also contribute to nonadaptive or maladaptive change by increasing the frequency of linked deleterious variants. Also, certain maladaptive alleles may have increased in frequency because of compensating fitness advantages they provide. Key Concepts: Reduced effective population size along the human lineage led to an increase in the influence of genetic drift and a reduction in the efficacy of natural selection, especially for mutations with small selective effects. Evidence for this can be seen in comparisons of measures of natural selection in lineages having different effective population sizes. Genome‐wide variation within and between human populations can be almost entirely explained by random drift and demographic forces other natural selection. Spatial expansions in human evolutionary history may cause gene surfing, in which low frequency alleles at the wave of advance can reach high frequencies and spread over large areas merely due to the effects of intense genetic drift. Nonadaptive gene surfing might be a better explanation than adaptive evolution for some high frequency, widespread genetic variants. Population bottlenecks in human evolutionary history can lead to increases in drift and reductions in the efficacy of purifying selection. This leads to an increase in the fraction of slightly deleterious mutations present in human populations that have experienced recent bottlenecks. Natural selection on alleles can result in nonadaptive shifts in the frequencies of alleles that are closely linked to them. Such linkage effects can lead to the increased frequencies of mildly deleterious alleles if they are linked to a beneficial variant, and can interfere with the effectiveness of adaptive evolution in promoting an advantageous allele if it is linked to a deleterious allele. Caution should be exercised in interpreting patterns of genetic variation in human populations as being adaptive without thoroughly ruling out nonadaptive explanations.