Drift on holey landscapes as a dominant evolutionary process

Abstract

An organism's 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 are 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 six 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.

Keywords: G matrix; evolutionary constraints; fitness landscapes.

Fig. 1.

Example fitness landscapes. Redder colors correspond to higher fitness. (A) A simple Gaussian, single peak Fujiyama landscape with a single optimum. (B) A more rugged landscape with multiple local optima and a single global optimum. (C) A simplified Holey landscape where combinations of values correspond to high, average, fitness (1) or low (0) fitness. This landscape has a large cluster of viable phenotypes with a hole and irregular borders and a smaller cluster of viable phenotypes at low trait values.

Fig. 2.

Modified “Orchard plot” of ${\lambda }_2/{\lambda }_1$ values for simulated (above solid line) and observed G matrices. Trunks (large points) are the medians for the specified group (e.g., Gaussian landscapes or Insecta), branches (thick lines) are interquartile ranges, twigs (thin lines) give the full range of values, and fruits (smaller points) are individual estimates within a simulation or taxonomic group. Rightmost letters correspond to statistical significance—or lack thereof—of comparisons of ratios among simulations. Datasets sharing letters did not significantly differ (SI Appendix, Table S3). Populations evolving due to drift alone had a significantly higher ratio than observed for either stabilizing selection or evolution on any of the holey landscapes. Populations evolving on holey landscapes also had lower ratios than those experiencing stabilizing selection but did not differ from each other. Rightmost numbers are the number of estimates available via literature search. (organism silhouettes courtesy of phylopic.org, Public Domain Mark 1 licenses or CCA 3.0; Chlorophyceae: S.A. Muñoz-Gómez, Superrosid: D.J. Bruzzese, Superasterid: T.M. Keesey and Nadiatalent).