Breeding Systems in Gymnosperms -- Relative Benefits and Costs of Being Monoecious or Dioecious

To start, a couple of definitions:

Dioecious plants are either male or female. Each individual plant, when it produces reproductive structures, produces only male or female structures.

Monoecious plants are both male and female. In gymnosperms, this means that the plant bears both male and female reproductive structures. Generally, the male and female reproductive structures are located in different parts of the plant, and/or become fertile at different times, to minimize the risk that the plant will reproduce with itself (this would largely negate the whole point of sexual reproduction, which is gene recombination). For instance, most monoecious conifers bear seed cones in the upper crown and pollen cones in the lower crown.

The question of which gymnosperms are monoecious and which dioecious was treated in encyclopedic manner by Givnish (1980). Other work, such as that by Adams (2018), has further shown us that there are many intermediate states, e.g. a dioecious population may contain some proportion of monoecious plants, or vice-versa, and that proportion may vary from less than 1% to nearly 50%, though the great majority of species are in the "less than 1%" group. In some taxa of Juniperus, one infraspecific taxon is monoecious and another dioecious.

Animal-dispersed gymnosperms are usually dioecious and wind-dispersed gymnosperms are usually monoecious. This correlation between breeding system and dispersal syndrome confers a disproportionate advantage in seed dispersal for plants with exceptionally large seed crops. Dioecy should be rare in herbs and shrubs; in plants whose flowers or floral rewards are large relative to the costs of pollen and seed production; in plants with flowers adapted to specialized, efficient movers of pollen; in species with wind-dispersed seeds; and in animal-dispersed species where seed dispersal is relatively independent of the number of seeds produced. These principles are supported by the distribution of breeding, pollination, and dispersal systems in various groups of seed plants (Givnish 1980).

Table 1 below is based strongly on Table 1 from Givnish (1980), with some more current information from Eckenwalder (2009) and Adams (2018), reformatted for conciseness and updated to contemporary taxonomy.

Table 1. Gymnosperm breeding systems and dispersal syndromes. Number of species in each taxonomic group indicated in parentheses.

Family	Genera	Breeding System	Dispersal Syndrome
Cycadaceae	Cycas (88)	Dioecious	Fleshy seeds; rarely, water-dispersed
Stangeriaceae	Bowenia, Stangeria (3)	Dioecious	Fleshy seeds
Zamiaceae	All (168)	Dioecious	Fleshy seeds
Araucariaceae	Araucaria, Section Araucaria (2)	Mostly dioecious	Winged cone scales
Araucariaceae	Agathis, Araucaria (sections other than Araucaria), Wollemia (38)	Monoecious	Winged cone scales
Cupressaceae	Juniperus (80% of taxa)	Dioecious	Fleshy cone
Cupressaceae	Juniperus (20% of taxa)	Monoecious	Fleshy cone
Cupressaceae	Austrocedrus, Diselma, Fitzroya (3)	Dioecious	Winged seed
Cupressaceae	All except Juniperus and Austrocedrus, Diselma, Fitzroya (84)	Monoecious	Winged seed
Pinaceae	Abies, Cathaya, Cedrus, Larix, Keteleeria, Nothotsuga, Picea, Pseudolarix, Pseudotsuga, Tsuga, and most Pinus (216)	Monoecious	Winged seeds
Pinaceae	Pinus subsections Cembroides and Rzedowskiae, plus P. albicaulis, P. cembra, and P. pinea (15)	Monoecious	Seeds with a very small or vestigial wing, animal-dispersed
Podocarpaceae	Acmopyle, Afrocarpus, Dacrycarpus, Falcatifolium, Nageia, Pherosphaera, Podocarpus, Pectinopitys, Prumnopitys, Retrophyllum, Sundacarpus (146)	Dioecious	Fleshy epimatium
Podocarpaceae	Dacrydium, Halocarpus, Lagarostrobos, Lepidothamnus, Manoao, Microcachrys, Parasitaxus, Phyllocladus, Saxegothaea (37)	Monoecious	Fleshy epimatium
Sciadopityaceae	Sciadopitys (1)	Monoecious	Winged seed
Taxaceae	All (28)	Dioecious	Fleshy arils or seeds
Ginkgoaceae	Ginkgo (1)	Dioecious	Fleshy seeds
Ephedraceae	Ephedra (61)	Mostly dioecious	Fleshy cone bracts, wind-dispersed in 8 spp, otherwise animal-dispersed
Welwitschiaceae	Welwitschia (1)	Dioecious	Conspicuous strobili with winged seeds
Gnetaceae	Gnetum (32)	Dioecious	Fleshy seeds

Table 1 does not address pollination, presumably because Givnish (1980) believed all gymnosperms to be wind-pollinated; however, we now know that some cycads are also pollinated by insects, particularly beetles. All such species are dioecious, bearing seeds covered in a fleshy integument. Table 1 indicates that there are 588 dioecious and 391 monoecious species of gymnosperms; this count assumes all Ephedra are dioecious. Nearly all of the dioecious species bear their seeds within a fleshy receptacle that is suitable for consumption by animals, indicating that animals are the primary dispersal agent in these species; only 2 species, Diselma and Welwitschia, are dioecious but bear winged seeds, which are readily dispersed by wind. Diselma is native to the Tasmanian alpine country, and Welwitschia is native to the Namibian desert; both are places where wind is a singularly potent dispersal mechanism due to frequent high wind velocities and large expanses of open country. Conversely, nearly all monoecious species have winged seeds that are readily dispersed by the wind; the exceptions are a group of 37 species in the Podocarpaceae; and 15 species of Pinus in which the seed wing has been reduced to the point where it serves little functional purpose, and the plants rely upon animals for seed dispersal.

The questions remain, why are some gymnosperms monoecious and others dioecious; why are some dispersed by animals and others by the wind; and why does monoecy tend to accompany wind dispersal, while dioecy accompanies animal dispersal? A variety of hypotheses can be advanced, but I can find no evidence of experimental confirmation. Here are some points in the discussion:

• Wind-dispersed seeds tend to be very light in weight and to be produced in large numbers, relative to animal-dispersed seeds. To put it another way, a plant can invest the same amount of resources and energy to produce a large number of wind-dispersed seeds, or a smaller number of animal-dispersed seeds.
• In at least some cases, animal-dispersed seeds can be shown to have an improved chance of survival, relative to wind-dispersed seeds. This occurs for two reasons. One is that the animals have coevolved a mutualistic relationship with the conifers, in that the animals place the seeds in locations where, if the animals don't eat them, the seeds have a good chance of germinating and eventually producing mature trees, thereby improving the food supply for the animals. This relationship has been conclusively demonstrated for many pines that produce large seeds with vestigial wings, and also appears to be well supported for certain junipers, podocarps, and yews, all of which are primarily disseminated by birds. The second reason is simply that animal-dispersed seeds are larger and heavier than wind-dispersed seeds and thereby provide the seedling a longer period of growth before it must start producing all of its own food through photosynthesis; this adaptation gives it a competitive advantage over small seeds.
• Ecological setting may favor either monoecy or dioecy. For instance, in an environment where plants may be isolated on the landscape, especially during dispersal events, the potential for self-fertilization in a monoecious plant may outweigh the genetic liabilities (primarily, inbreeding depression) of such a strategy, enabling a single plant to generate a new population. Conversely, in an environment where plants are densely distributed on the landscape, dioecy ensures a minimal risk of inbreeding and opens the possibility of sex ratio adjustment, e.g. more female plants increase reproductive potential whereas more male plants increases the potential for long-distance dispersal of genetic material. Thus a dioecious plant may be more adaptable to a changing environment.
• Ecological setting may also favor either wind or animal dispersal. In a desert or alpine setting, trees may experience frequent high winds that favor wind dispersal as an effective way of expanding extant populations and establishing new ones via dispersal. In a rainforest, though, high winds may be uncommon, dispersal of larger seeds may be needed to overcome competition effects on seedlings, and it may be highly beneficial to have a coevolved animal disperser that will deliver seeds to suitable germination sites.
• Monoecy and dioecy seem to be conservative traits; they are usually consistent within a genus and even conifer families tend to show broadly consistent trends towards monoecy or dioecy. Thus these traits show slow or no tendency to change over evolutionary time. Conversely, the transition between wind and animal dispersal appears to be relatively plastic, requiring only a gradational change in seed mass or size of a seed wing. This can be seen in Pinus, where a continuum of seed weight and seed wing length can be seen between clearly wind-dispersed species and clearly animal-dispersed species; Pinus flexilis, for example, is a highly intermediate species with a seed that is too heavy and a wing too small for effective wind dispersal (except by very strong winds, which do tend to occur in places where this species grows), and a seed that is large enough to attract animal dispersers, who tend to cache the seeds in sites suitable for germination.

Citations

Adams, Robert P. 2018. Evolution of dioecious/monecious taxa in Juniperus, contrasted with Cupressus, Hesperocyparis, Callitropsis and Xanthocyparis (Cupressaceae). Phytologia 100(4):248-255.

Givnish, Thomas J. 1980. Ecological contraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. Evolution 34(5):959-972.