Breeding Systems

Breeding systems in plants refer to the variety of ways plants answer the general question of "Who mates with whom" by answering specific questions such as whether flowers mature at the same time, whether a plant has more than one kind of flower or differs from other plants in types of flowers, and whether there are chemicals that keep certain plants from mating with each other.

Outcrossing and Inbreeding

Most vertebrate species consist of separate male and female individuals. In contrast, the majority of flowering plants are hermaphroditic, with both pollen and ovules produced by the same plant. As a consequence, many flowering plants are capable of self-fertilization (selfing), with seeds resulting from pollen and eggs produced by the same plant. The self pollen that fertilizes the egg may be produced by the same flower (called autogamy) or by different flowers on the same plant (geitonogamy). Selfing or mating among close relatives (inbreeding) often results in offspring that have reduced vigor and produce fewer offspring compared to offspring from matings between unrelated plants (outcrossing). This reduction in fitness of selfed offspring relative to outcrossed offspring is referred to as inbreeding depression. If both selfing levels and levels of inbreeding depression are high, natural selection may favor mechanisms that promote outcrossing. High levels of inbreeding depression are likely to be found in populations that have been outcrossing for a long time. In contrast, in populations that have been inbreeding (high selfing rates) for many generations, inbreeding depression levels may now be low because harmful genes have already been eliminated from the population by natural selection.

Selfing may also have direct advantages. Selfing plants may have an automatic selection advantage and contribute more genes to the next generation because they contribute both maternal genes (through the egg) and paternal genes (through pollen) to selfed seeds, and they also contribute pollen (and thus paternal genes) to other plants, spreading their genes further. In contrast, outcrossing plants contribute pollen to other plants, but only maternal genes to their own seeds. This automatic selection advantage will lead to selection for selfing if selfing does not decrease outcrossing (thereby limiting the spread of genes), and if inbreeding depression is not too severe. In addition, selfing tends to produce offspring more similar to the parent plant than outcrossing. If seeds are dispersed locally into habitat similar to that of the parent, these selfed offspring may do better than outcrossed offspring. In habitats where pollen is limited because of low population density or because there are few pollinators, selfing may also provide reproductive assurance with a guaranteed source of pollen. Some plants, such as touch-me-not (Impatiens ) and some violet species (Viola ) have evolved flowers that are pollinated autogamously and never open (called cleistogamy), as well as the more showy open flowers (chasmogamy).

Heterostyly

Several factors may promote outcrossing, including separation of male and female function in time or space. In heterostylous plants such as the primrose (Primula ) described by English naturalist Charles Darwin (1809-1882), there are two floral forms (distyly). In one form, pin flowers have long styles and short stamens. Thrum flowers have short styles and long stamens. This positioning favors outcrossing with transfer of pollen between the pin and thrum plants by pollinators.

Dichogamy

In dichogamy, pollen is released and the stigma is receptive (ready to receive pollen) at different times. There are two types: in protandry ("early male"), the pollen is shed before the stigmas are receptive, while in protogyny ("early female"), the stigmas are receptive before the pollen is shed. Even greater outcrossing is promoted by synchronizing all of the flowers on the plant for the same sex, so that all stigmas are receptive together, either before or after all pollen is shed.

Dioecy

Spatial separation of the sexes onto different flowers or different plants may also promote outcrossing. An individual flower may have only stamens (male) or only pistils (female), or both (hermaphroditic) in the same flower, and plants and populations may have various combinations of flowers. Monoecious ("one house") populations have both sexes of unisexual flowers on each plant (e.g., corn has tassels of male flowers and an ear of female flowers on the same plant). Gynodioecious populations, consisting of female and hermaphroditic plants, are also possible. Dioecious ("two-house") populations consist of male-only and female-only plants (e.g., marijuana, or Cannabis ). Dioecy has arisen independently in the flowering plants many times. About 6 percent of flowering plant species are dioecious, and the incidence of dioecy is particularly high in the Hawaiian Islands (14.7 percent) and in New Zealand (12 to 13 percent). Flowering plants also have more complicated patterns of sex expression, and some plants are even capable of switching sex through time.

Two major theories have been proposed to explain the evolution of dioecy. One theory suggests that dioecy has evolved as a mechanism to avoid inbreeding depression and enforce outcrossing between unisexual plants. The other theory suggests that patterns of resource allocation between male and female function (sex allocation) are critical. According to this theory, dioecy should evolve from hermaphroditism when greater investment of resources in flowers of one sex yields a disproportionate gain in reproductive success. In such cases, it would be advantageous to separate the sexes to allow more efficient resource allocation.

Self-incompatibility

Even without spatial or temporal (time-related) separation, chemical incompatibility between the stigma or style and pollen of the same plant can also promote outcrossing. Molecular data suggest that self-compatibility is the ancestral condition in flowering plants and that self-incompatibility has evolved independently many times. In plants such as tobacco (Nicotiana ) that have gametophytic self-incompatibility (GSI), pollen tubes germinate but fail to grow through the style if they are chemically incompatible. In GSI, the incompatibility reaction is determined by the combination of the self-incompatibility (SI) genes of the maternal plant and the SI genes of the pollen grain. GSI is found in several species, including tobacco and some grasses.

In sporophytic self-incompatibility (SSI), the incompatibility reaction is controlled by the combination of maternal plant SI genes in the stigma and the SI genes of the plant that produced the pollen, rather than those of the pollen grain itself. Incompatible reactions cause the pollen tube to stop growing on or near the stigma. Multi-allelic SSI systems have many incompatibility types, and proteins that cause the incompatibility reaction are produced by the anthers and are present in the outer layer of the pollen grain. Broccoli and many other members of the mustard family (Brassicaceae) have multi-allelic SSI.

In contrast, many plants with SSI have only two or three incompatibility types, but are heterostylous (e.g., shamrock [ Oxalis ], and water hyacinth [ Eichhornia ], a noxious, invasive aquatic weed).

see also Flowers; Pollination Biology; Reproduction, Asexual; Reproduction, Fertilization and; Reproduction, Sexual; Seed Dispersal.

Ann K. Sakai

Bibliography

Bertin, Robert I. "Pollination Biology." In Plant-Animal Interactions. Warren G. Abrahamson, ed. New York: McGraw-Hill, 1989.

Briggs, D., and S. M. Walters. Plant Variation and Evolution, 3rd ed. Cambridge, UK:Cambridge University Press, 1997.

Sakai, Ann K., and Stephen G. Weller. "Gender and Sexual Dimorphism in Flowering Plants: A Review of Terminology, Biogeographic Patterns, Ecological Correlates, and Phylogenetic Approaches." In Sexual and Gender Dimorphism in Flowering Plants, eds. Monica A. Geber, Todd E. Dawson, and Lynda F. Delph. Heidelberg: Springer-Verlag, 1999.