ECOLOGICAL CONSTRAINTS ON THE EVOLUTION OF BREEDING SYSTEMS IN SEED PLANTS: DIOECY AND DISPERSAL IN GYMNOSPERMS

Studies on the evolution of breeding systems have recently focused on the adaptive significance of dioecy vs. monoecy and hermaphroditism in plants (Ross, 1970; Lloyd, 1972, 1975; Bawa, 1974; Arroyo and Raven, 1975; Bawa and Opler, 1975, 1978; Ross and Weir, 1975; Ashton, 1976; Charnov et al., 1976; Freeman et al., 1976; Melampy and Howe, 1977; Charlesworth and Charlesworth, 1978; Zapata and Arroyo, 1978; Charnov, 1979; Opler, 1979; Willson, 1979). Dioecy is marked by the presence of male and female flowers on separate plants; monoecy, by the presence of male and female flowers on the same plants; and hermaphroditism, by the presence of perfect, or bisexual, flowers on all plants. Whereas dioecy, or separation of the sexes, is frequent in animals and especially vertebrates, it is relatively uncommon in flowering plants (Maynard Smith, 1978). Although 22-40% of woody species are reported dioecious in certain tropical floras, the incidence of dioecy is less in temperate trees, and much less in temperate shrubs and herbs (Bawa and Opler, 1975). Several conflicting views have been advanced as to what ecological and evolutionary factors may favor dioecy (Darwin, 1877; Mather, 1940; Lewis, 1942; Stebbins, 1951; Baker, 1958; Ornduff, 1966; Opler and Bawa, 1978; and references cited above). Gymnosperms have been largely ignored in this controversy, but their combination of breeding, pollination, and dispersal systems casts important light on the evolution of dioecy. Most gymnosperms are either monoecious or apparently dioecious, although a few species have populations with both monoecious and dioecious members (Pilger, 1926; Pearson, 1929; Florin, 1933, 1958; Chamberlain, 1935; Cutler, 1939; Martinez, 1946; Hunziker, 1949; Buchholz and Gray, 1958; Johnson, 1959; Marsh, 1966; Dallimore et al., 1967; Mirov, 1967; Keng, 1969, 1978; deLaubenfels, 1969, 1972, 1978a, 1978b; Veillon, 1978). All gymnosperms are wind-pollinated (see Giddy, 1974, regarding alleged beetle pollination in cycads), but two major dispersal syndromes are known. One involves wooden or leathery cones enclosing (usually) winged seeds that are windor gravity-dispersed. The other involves fleshy, often showy "fruits" or arils surrounding wingless seeds that are animal-dispersed. The term "fruit" is used in an ecological and functional sense in this paper; gymnosperm "fruits" actually represent a great diversity of morphologically distinct, but ecologically similar, structures that attract seed dispersers. The distribution of dispersal syndromes among the 804 extant species in 14 gymnosperm families and 74 genera is shown in Table 1. The striking pattern that emerges is that, with mode of pollination controlled, breeding system correlates almost perfectly with dispersal syndrome (Table 2). Almost all cone-bearing species, with winddispersed seeds, are monoecious and almost all species with fleshy or showy fruits, dispersed by animals, are dioecious. To a certain extent, this pattern is set by familiar specialization: most species in the Araucariaceae, Pinaceae, and Taxodiaceae are monoecious and wind-dispersed, while most in the Cycadaceae, Stangeriaceae, Zamiaceae, Ginkgoaceae, Taxaceae, Cephalotaxaceae, Podocarpaceae, Ephedraceae, and Gnetaceae are