A novel cost framework reveals evidence for competitive selection in the evolution of complex traits during plant domestication
AbstractMost models of selection incorporate some notion of an environmental degradation in which the majority of the population becomes less fit with respect to a character resulting in a pressure to adapt. Such models have been variously associated with an adaptation cost, the substitution load. Conversely, adaptative mutations that represent an improvement in fitness in the absence of environmental change have generally been assumed to be associated with negligible cost. However, such adaptations could represent a competitive advantage that diminishes resource availability for others and so induce a cost. This type of adaptation in the form of seedling competition has been suggested as a mechanism for increases in seed size during domestication. Here we present a novel cost framework for competitive selection that demonstrates significant differences in behaviour to environmental based selection in typical initial selection intensity and intensity over time. We show that selection intensity over time in grain size metrics of nine archaeological crops increases in one to several episodes fitting closely to the competitive selection model of single large effect alleles, but surprisingly in direct contrast to the expectations of the standard model of stabilizing selection. While size trait changes ultimately slow down in crops over time as expected from pleiotropic constraints expressed in the standard model, the mechanism outlined here shows possible complexities within the environmental based mode of shifting optimums in the standard model and a fundamental insight into the factors driving domestication.Significance statementWe present here a new model framework for selection based on direct competition between individuals rather than the more conventional approach of individual’s fitness being measured against an environmental gradient. The model explains patterns of increasing selection intensity seen in archaeological grain sizes of nine domesticated crops that otherwise contradict the expectations of shifting stabilising selection of complex traits. We show that grain size increases seen across domesticated crops are consistent with spontaneous competition between seedlings under cultivation for resources and so reveal a fundamental insight into the mechanism of plant adaptation to the human environment.
