Dioecy

Abstract: Dioecy, characterized by the presence of distinct male and female plants, is widespread in angiosperms, being known in 37 out of Engler & Prantl's 51 orders (132). Yet botanists have paid little attention to dioecy, particu­ larly to selective forces underlying its evolution. Several factors have con­ tributed to this neglect. First, though there are many dioecious species, the proportion of such species in the world's flora is reputed to be quite small (37, 53, 132). The presumed rarity of the dioecious condition has led to the belief that it is not a particularly successful mode of reproduction (53, 125). Second, dioecy has been compared with self-incompatibility and, because 50% of the dioecious plants lose the capacity to bear seeds, it has been considered a poor substitute for self-incompatibility (3, 53). Third, selection for outcrossing has been almost universally proposed as the principal selec­ tive force responsible for the evolution of dioecy (3, 16-18, 26, 45, 67, 84-86, 98, 101, 103). The proposal has little empirical support, but one of its consequences was that biologists took for granted the outcrossing advantage as the principal factor and, until recently (10, 21, 128), did not consider other factors influencing the evolution of dioecy. I wish to argue that dioecy is not as rare as is generally assumed. In certain regions, among certain life forms, more than one fourth of all species may be dioecious (see below). In addition, I argue that the evolution of dioecy is not entirely due to selective pressure for increased outcrossing. By

Abstract: Considerable ffort has been spent documenting correlations between dioecy and various ecological and morphological traits for the purpose of testing hypotheses about conditions that favor dioecy. The data analyzed in these studies, with few exceptions, come from local floras, within which it was possible to contrast he subsets of dioecious and nondioecious taxa with regard to the traits in question. However, if there is a strong phylogenetic component o the presence or absence of dioecy, regional sampling may result in spurious associations. Here, we report results of a categorical multivariate analysis of the strengths ofvarious associations of dioecy with other traits over all flowering plants. Families were scored for presence of absence of monoecy or dioecy, systematic position, numbers of species and genera, growth forms, modes of pollination and dispersal, geographic distribution, and trophic status. Seven percent of angiosperm genera (959 of 13,500) contain at least some dioecious species, and ;6% of angiosperm species (14,620 of 240,000) are dioecious. The most consistent associations in the data set relate the presence of dioecy to monoecy, wind or water pollination, and climbing rowth. At both the family and the genus level, insect pollination is underrepresented among dioecious plants. At the family level, a positive correlation between dioecy and woody growth results primarily from the association between dioecy and climbing growth (whether woody or herbaceous) because neither the tree nor the shrub growth forms alone are consistently correlated with a family's tendency to include dioecious members. Dioecy appears to have evolved most frequently via monoecy, perhaps through divergent adjustments of floral sex ratios between individual plants. Monoecy itself is related to abiotic pollination and climbing rowth as revealed by multivariate analysis. Dioecy and monoecy are concentrated in the less advanced superorders of Thorne (1992) and subclasses of Cronquist (1988). The frequency of dioecy found in a local flora therefore flects the level of dioecy in its particular pool of families as much as, or more than, local selective factors. The positive associations of dioecy with abiotic pollination and monoecy are related to floral developmental nd morphological attributes, as is the negative association with bird and bat pollination; the positive association of dioecy with climbing growth is tentatively explained in terms of differential se ection for optimal resource allocation to sexual function. If rapid upward growth is at a premium in climbers and if fruit set at least temporarily inhibits growth or requires the production of thicker, more slowly growing stems to support heavy fruits, itmight be advantageous to postpone femaleness. Ifthe effect is strong, this may favor male plants.

Abstract: Publisher Summary Dioecism has arisen independently in different plant families and plant genera. In the majority of cases, the evolution of dioecism has apparently taken place on the species level; in some cases, on the subgeneric level (rumex) or generic level (humulus). Few families (salicaceae) comprise only dioecious species. Dioecious plants offer, in many cases, better tools for studying the genetics of sex determination than dioecious animals. First, the fact that dioecious plants have arisen independently gives an opportunity to study the different ways in which dioecism may become established. Second, in plants the step from dioecism to bisexuality is often a short one and in most cases, dioecism is not clear-cut. In many dioecious species (e.g. mercurialis), bisexual types are found in nature often with a rather high frequency. Such bisexual individuals of normally dioecious plant species are almost always fertile and can be genetically studied, whereas similar bisexual animals are sterile intersexes. In plants it is possible to follow both the evolution of dioecism from hermaphroditism (or monoecism) and the reverse process.

Abstract: UNLABELLED • PREMISE OF THE STUDY Separating sexual function between different individuals carries risks, especially for sedentary organisms. Nevertheless, many land plants have unisexual gametophytes or sporophytes. This study brings together data and theoretical insights from research over the past 20 yr on the occurrence and frequency of plant sexual systems, focusing on the flowering plants.• METHODS A list of genera with dioecious species, along with other information, is made available (http://www.umsl.edu/∼renners/). Frequencies of other sexual systems are tabulated, and data on the genetic regulation, ecological context, and theoretical benefits of dioecy reviewed.• KEY RESULTS There are 15600 dioecious angiosperms in 987 genera and 175 families, or 5-6% of the total species (7% of genera, 43% of families), with somewhere between 871 to 5000 independent origins of dioecy. Some 43% of all dioecious angiosperms are in just 34 entirely dioecious clades, arguing against a consistent negative influence of dioecy on diversification. About 31.6% of the dioecious species are wind-pollinated, compared with 5.5-6.4% of nondioecious angiosperms. Also, 1.4% of all angiosperm genera contain dioecious and monoecious species, while 0.4% contain dioecious and gynodioecious species. All remaining angiosperm sexual systems are rare. Chromosomal sex determination is known from 40 species; environmentally modulated sex allocation is common. Few phylogenetic studies have focused on the evolution of dioecy.• CONCLUSIONS The current focus is on the genetic mechanisms underlying unisexual flowers and individuals. Mixed strategies of sexual and vegetative dispersal, together with plants' sedentary life style, may often favor polygamous systems in which sexually inconstant individuals can persist. Nevertheless, there are huge entirely dioecious clades of tropical woody plants.