Adaptive excursions across the drift barrier

Random genetic drift, rather than selection, is expected to determine the dynamics of alleles with fitness effects that fall below the reciprocal of effective population size (Ne). This is the drift barrier. The drift barrier hypothesis suggests that adaptation may be hopelessly constrained in organisms with low Ne, with much of the complexity of life reflecting a byproduct of ineffective natural selection. Yet decades of empirical research in evolutionary ecology provides substantial evidence of adaptation in finite metazoan populations. Here I explore the extent to which the drift barrier may, or may not, constrain contemporary adaptive divergence under directional selection in the wild. Compensatory directional selection on polygenic traits occurring after the fixation of a deleterious allele will be twice as efficient compared to the initial action of stabilizing selection. Consistent with this result, meta analysis reveals a negative relationship between contemporary estimates of Ne and the strength of directional selection in natural populations. Analysis of empirical phenotypic selection gradients from wild metazoans further reveals that directional selection is often strong enough to overcome the constraints imposed by finite population size, across a range of genetic architectures. Moreover, on a multi-peak adaptive landscape, the probability of a peak shift between adaptive zones increases exponentially as Ne declines, with observed values of contemporary Ne typically being well within the range needed for peak shift models to be a viable explanation of diversity. Together, these results suggest that widespread adaptation in metazoans is not inconsistent with the fundamental constraints on perfection imposed by drift.