THE EVOLUTION OF OUTCROSSING IN HIGHER PLANTS, WITH SPECIAL REFERENCE TO THE EVOLUTION OF DISTYLY

Abstract

Models are developed for the evolution of outcrossing in general and the evolution of distyly in particular. Field studies of distylous Lithospermum cobrense (Boraginaceae) are reported to support and compliment theoretical work. First a method is developed to model selection against selfing which takes into account the effects of consecutive generations of selfing on loss of heterozygosity. Conditions are then derived for optimal rates of outcrossing. Intermediate rates of outcrossing are optimal under a wide range of parameter values. One assumption of this model is that seedset is not pollen-limited. I then investigate the nature of inherent constraints on whether seedset is pollen-limited or resource-limited in outcrossing animal-pollinated plants, and conclude resource limitation is likely when the per-seed cost of fruit production is greater than the per-seed cost of pollen production. The model also points to why animal-pollinated plants usually have hermaphrodite flowers. This model is followed by analyses of pathways for the evolution of self-incompatibility with two mating types such as is associated with distyly. To account for this I show it necessary to postulate a fortuitous conjunction of rare mutations, very severe selection against selfing, and/or unusual mutational effects. It is also necessary to postulate resource-limited seedset. At this point I develop models for floral differentiation of mating types, culminating in the completely distylous condition. Once self-incompatibility has evolved in plants with stigmas and anthers already spatially separated, it is possible to account for complete floral differentiation under both pollen limitation and resource limitation. Field studies of L. cobrense focus on the pattern of pollen dispersal by butterflies, the mechanism accounting for this pattern, and the extent to which this pattern leads to resource or pollen limitation of seedset. In this species and in distylous species generally, the major effect of reciprocal placement of anthers and stigmas in the two mating types is to enhance the efficiency with which pollen is transported to compatible stigmas. This enhances male fitness but for full distyly to evolve it is helpful, though not strictly necessary, for female fitness to be affected too, as under pollen limitation. Finally, I argue that sporophytically controlled multiallelic self-incompatibility may originate by pathways similar to those envisioned for distyly, and that these two kinds of breeding systems are branches with a common stem.