THE EVOLUTION OF GYNODIOECY AND SUBDIOECY

Darwin (1877) attempted to understand the significance and evolution of unisexuality in plants. In addition to dioecy, he recognized gynodioecy, in which separate female and hermaphrodite individuals are found, androdioecy, where there are males and hermaphrodites, and several other conditions. Most of the gynodioecious species studied by Darwin were members of the Labiatae, with one or a few species in other groups, such as the genera Scabiosa, Plantago and Cirsium (then called Cnicus). These species rarely showed any tendency to be dioecious. Since especially the Labiatae contain many gynodioecious and many hermaphroditic species but few dioecious ones, Lewis (1942) concluded that there was little evidence for an evolutionary connection between gynodioecy and dioecy. Such a conclusion is in accord with most of the then available evidence, but recent studies have shown that there are groups of related species of which some are gynodioecious and others are dioecious or nearly so, e.g. in Pimelea (Burrows, 1960; Ross, 1970b) and in New Zealand Umbelliferae (Lloyd, 1973). In one section of the genus Fuchsia three species are morphologically gynodioecious but functionally subdioecious (Arroyo and Raven, 1975). Since these groups have hermaphrodite relatives it seems that gynodioecy first evolved from hermaphroditism and then gave rise to near dioecy by gradual reduction of seed fertility of hermaphrodites. Consequently we may now recognize two evolutionary types of gynodioecy, namely a stable or classical type which rarely gives rise to dioecy, and an unstable type which appears to do so frequently. A model of the evolution of dioecy with male heterogamety through the development of complete linkage between a recessive gene m for male sterility, and a dominant gene F for female sterility, was presented by Lewis (1942). Males had genotype MF/mf and females mf/mf, but if the dominance of the two mutations was reversed, females would be heterogametic. Studies of gene substitutions in populations under Lewis' model with male heterogamety showed that dioecy could evolve, but only with large selection differentials (Ross and Weir, 1976). This result, together with the evidence that subdioecy evolved from gynodioecy by gradual reduction of seed set on hermaphrodites, suggested that a new hypothesis for the evolution of dioecy was required. Ross and Weir (1976) proposed a multilocus hypothesis with several recessive genes for male sterility and dominant or nondominant genes for partial female sterility. Valdeyron (1972) also proposed a multilocus control of female sterility in a subdioecious species, and Westergaard (1958) has inferred the presence of two male-sterility genes in Melandrium. The present paper has two main aims. First it aims to test Ross and Weir's hypothesis by studying a recessive gene for male sterility and a nonrecessive gene for partial female sterility. It is shown that there are interactions such that even without linkage there may be more females in equilibrium populations in the presence of partially female-sterile hermaphrodites ("subhermaphrodites") than in their absence, and vice versa. Linkage results in increased proportions of females and subhermaphrodites, and decreased proportions of hermaphrodites. It is held that additional mutations would behave in the same way. making the evolution of sub-