The origin and function of self-incompatibility in flowering plants

Summary The evolutionary significance of self-incompatibility (SI) traditionally has been linked to reduced inbreeding through enforced outcrossing. This view is founded on the premise that outcrossing reduces inbreeding. It is important, when considering the evolutionary significance of any genetic system, to try to distinguish those factors related to the evolution of, from those related to the maintenance of, the system in question. Three factors are considered important for the maintenance of SI: (1) phylogenetic constraint in species descended from SI ancestors, (2) reduced inbreeding in populations, and (3) fitness benefits to individuals resulting from the avoidance of selfing. I suggest that the first two factors should be rejected when considering the origin of SI (whether one or more origins are hypothesized) and that the increase in individual fitness resulting from the avoidance of self-fertilization among individuals that are heterozygous for deleterious alleles may be sufficient to account for the origin of SI. Self-fertilization in plants (except in species that predominantly self-fertilize) generally results in a reduction in fitness of some individuals due to the increased expression of deleterious or lethal recessive alleles, regardless of the degree of inbreeding in the population or the frequency of the allele in question. Inbreeding is a consequence of population structure in many outcrossing plant species. Complex (multi-locus and multi-allelic) systems of SI exist that reduce inbreeding. However, it is argued that these are derived either from simpler systems of SI that may have very little or no effect on inbreeding, in which case any effect on level of inbreeding is secondary, or are not true self-incompatibility systems and are part of a regulatory system that serves to balance the level of inbreeding and outbreeding. Multi-locus and multi-allelic systems of SI and heteromorphic systems of SI are discussed in terms of derived versus ancestral characteristics. A reassessment of the role of breeding systems in the development of a population structure promoting inbreeding is suggested, which may have been of crucial importance in the success and diversification of angiosperms.