Loss of Self‐Incompatibility and Its Evolutionary Consequences

Abstract

We review and analyze the available literature on the frequency and distribution of self‐incompatibility (SI) among angiosperms and find that SI is reported in more than 100 families and occurs in an estimated 39% of species. SI frequently has been lost but rarely has been gained during angiosperm diversification, and there is no evidence that any particular system of SI, once lost, has been regained. Irreversible loss of SI systems is thought to occur because transitions to self‐compatibility (SC) are accompanied by collapse of variation at the S‐locus and by accumulation of loss‐of‐function mutations at multiple loci involved in the incompatibility response. The asymmetry in transitions implies either that SI is declining in frequency or that it provides a macroevolutionary advantage. We present a model in which the loss of SI is irreversible and species can be SI, SC but outcrossing, or predominantly selfing. Increased diversification rates of SI relative to SC taxa are required to maintain SI at equilibrium, while transition rates between states, together with state‐specific diversification rates, govern the frequency distribution of breeding‐system states. We review empirical studies about the causes and consequences of the loss of SI, paying particular attention to the model systems Arabidopsis and Solanum sect. Lycopersicon. In both groups, losses of SI have been recent and were accompanied by loss of most or all of the functional variation at the S‐locus. Multiple loss‐of‐function mutations are commonly found. Some evidence indicates that mutations causing SC strongly increase the selfing rate and that SC species have lower genetic diversity than their SI relatives, perhaps causing an increase in the extinction rate.