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Substitution load imposes a mild constraint on adaptation, with a high proportion of deaths in A. thaliana being selective


Authors:
Joseph Matheson 1; Moises Exposito-Alonso 2; Joanna Masel 1

Affiliations:
1) University of Arizona, Tucson, AZ; 2) Carnegie Institution for Science, Stanford University, Stanford, California

Keywords:
Natural selection

Haldane (1957) argued that the need for a minimum number of “selective deaths” over the course of an adaptive substitution acts as a limit to the speed of adaptation. He estimated that mammalian species could only sustain one adaptive substitution every 300 generations. The fact that substitutions occur much faster than this limit was the original argument put forward in favor of neutral theory. However, while most population geneticists today no longer consider Haldane’s argument to imply a serious limit to adaptation, there is no agreement as to the reasons why, nor what the true limit is. Many follow Maynard Smith (1968), attributing the resolution of the problem to an extreme form of synergistic epistasis, which there is now enough data to exclude. More plausible is that early load arguments mistakenly compared average fitness to the fitness of a perfectly adapted population (Ewens 1970), a mistake also corrected as part of Maynard Smith’s model. Here we disentangle multiple distinct lines of reasoning about the ambiguous term ‘substitution load’, including selective deaths, reproductive excess, and load sensu strictu. Importantly, while a variety of considerations do not meaningfully limit adaptation, reasoning based on selective deaths still can. We therefore applied the concepts of load and selective deaths to survival and fecundity data on 517 different genotypes of Arabidopsis thaliana grown in eight different environmental conditions. We estimate highly permissive limits to the speed of adaptation in all environmental conditions. While harsher environmental conditions decrease reproductive excess and hence the potential for selective deaths, this is compensated by higher proportions of deaths being selective. Selective deaths are more common than anticipated during historical discussions of speed limits. Less fecund species than Arabidopsis could nevertheless face meaningful limits to the speed of adaptation, especially in harsher environments where adaptation is most important.