EVOLUTION OF INCOMPATIBILITY SYSTEMS IN PLANTS: ORIGIN OF ‘INDEPENDENT’ AND ‘COMPLEMENTARY’ CONTROL OF INCOMPATIBILITY IN ANGIOSPERMS

SUMMARY Incompatibility is a common means of controlling breeding behaviour among plants, and has been an important factor in evolution. It acts to prevent self‐fertilization, as well as to prevent sterilization of ovules by foreign pollen. Angiosperms have both inter‐ and intraspecific incompatibility, and these are controlled by the same S gene complex. Gymnosperms, however, have only interspecific incompatibility. Observations on incompatibility behaviour in flowering plants have suggested that interspecific incompatibility evolved first among gymnosperms or progymnosperms as a means of protecting their naked ovules from foreign pollen. Duplication and redifferentiation of this ‘primary specificity’ gene in angiosperm precursors subsequently gave rise to ‘secondary specificity’ controlling intraspecific incompatibility. Today there are three basic types of incompatibility found among the angiosperms: (i) inherently independent control‐each allele independently expresses its individual specificity, shows allelic interaction in the pollen after S gene duplication; (ii) inherently complementary control‐alleles of two or more incompatibility loci co‐operate to produce a single specificity, shows no allelic interaction; and (iii) late complementary control‐alleles of two or more incompatibility loci co‐operate to produce a single specificity, shows allelic interaction. The pattern of distribution of these three types of control has given rise to a controversy over which represents the most primitive type of angiosperm incompatibility. The present paper examines the factors involved in secondary evolution of incompatibility, and concludes that independent control is in fact more primitive. Complementary control probably developed secondarily and independently several times during angiosperm evolution, the first occurrence, that of ‘inherently complementary’ apparently being among the progenitors of the monocotyledons. While the majority of dicotyledons have the original ‘inherently independent’ control, certain evolutionary lines appear to have switched independently to complementary control, the gametophytic system giving rise to ‘inherently complementary’ control and the sporophytic system giving rise to ‘late complementary’ control. A major factor in favour of complementary incompatibility system as opposed to independent control system is the advantage it confers in colonisation after long distance dispersal. The factors involved in the evolution of complementary control, together with certain genetic characteristics of this system, have probably played a significant role in the evolution and distribution of monocotyledons.