Drift on holey landscapes as a dominant evolutionary process

Abstract

An organisms phenotype has been shaped by evolution but the specific processes have to be indirectly inferred for most species. For example, correlations among traits imply the historical action of correlated selection and, more generally, the expression and distribution of traits is expected to be reflective of the adaptive landscapes that have shaped a population. However, our expectations about how quantitative traits--like most behaviors, physiological processes, and life-history traits--should be distributed under different evolutionary processes is not clear. Here we show that genetic variation in quantitative traits is not distributed as would be expected under dominant evolutionary models. Instead, we found that genetic variation in quantitative traits across 6 phyla and 60 species (including both Plantae and Animalia) is consistent with evolution across high dimensional "holey landscapes". This suggests that the leading conceptualizations and modeling of the evolution of trait integration fail to capture how phenotypes are shaped and that traits are integrated in a manner contrary to predictions of dominant evolutionary theory. Our results demonstrate that our understanding of how evolution has shaped phenotypes remains incomplete and these results provide a starting point for reassessing the relevance of existing evolutionary models. Significance StatementWe found that empirical estimations of how quantitative genetic variation is distributed do not correspond to typical Gaussian representations of fitness landscapes. These Gaussian landscapes underpin major areas of evolutionary biology and how selection is estimated in natural populations. Rather than being consistent with evolution on Gaussian landscapes, empirical estimates of genetic variation are, instead, consistent with evolution on high-dimensional "holey" landscapes. These landscapes represent situations where specific combinations of trait values are either viable or not and populations randomly drift among the viable combinations. This finding suggests that we have substantially misunderstood how selection actually shapes populations and thus how evolution typically proceeds.