Substitution load revisited: a high proportion of deaths can be selective.

Haldane's Dilemma refers to the concern that the need for many "selective deaths" to complete a substitution (i.e. selective sweep) creates a speed limit to adaptation. However, discussion of this concern has been marked by confusion, especially with respect to the term "substitution load". Here, we distinguish different historical lines of reasoning, and identify one, focused on finite reproductive excess and the proportion of deaths that are "selective" (i.e. causally contribute to adaptive allele frequency changes), that has not yet been fully addressed. We develop this into a more general theoretical model that can apply to populations with any life history, even those for which a generation or even an individual are not well defined. The actual speed of adaptive evolution is coupled to the proportion of deaths that are selective. The degree to which reproductive excess enables a high proportion of selective deaths depends on the details of when selection takes place relative to density regulation, and there is therefore no general expression for a speed limit. To make these concepts concrete, we estimate both reproductive excess, and the proportion of deaths that are selective, from a dataset measuring survival of 517 different genotypes of Arabidopsis thaliana grown in 8 different environmental conditions. In this dataset, a much higher proportion of deaths contribute to adaptation, in all environmental conditions, than the 10% cap that was anticipated as substantially restricting adaptation during historical discussions of speed limits.