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  • Review Article
  • Published:

Evolution of sex

The evolution of plant sexual diversity

Nature Reviews Genetics volume 3, pages 274–284 (2002)Cite this article

Key Points

  • Flowers, the reproductive organs of angiosperms, are more varied than the equivalent structures of any other group of organisms, and flowering plants also have an unrivalled diversity of sexual systems. This variation provides outstanding opportunities for evolutionary and functional studies of the costs and benefits of alternative sexual strategies.

  • The two main evolutionary transitions in sexual systems of flowering plants involve the shift from predominant outcrossing to predominant selfing, and the evolution of separate sexes from combined sexes. Comparative studies indicate that these transitions have originated independently on numerous occasions in angiosperm families.

  • Many floral mechanisms that have been traditionally interpreted as 'anti-selfing mechanisms' might have an alternative role in promoting fitness through male reproductive function by limiting gamete losses through pollen discounting. This is particularly likely in self-incompatible plants because they are already protected from the harmful effects of inbreeding by physiological mechanisms.

  • Sexual polymorphisms, such as heterostyly and enantiostyly, that are characterized by reciprocal herkogamy, function to increase the precision of animal-mediated cross-pollination, while reducing the costs that are associated with sexual interference between female and male sexual organs. The principal cost is pollen wastage through self-pollination.

  • The two main evolutionary routes for the origin of dioecy — the gynodioecy and monoecy pathways — differ in the types of gender variation on which selection acts, and in the relative importance of major versus minor genes that govern changes to sexuality. The fitness consequences of selfing and outcrossing, and the optimal allocation of resources to female and male function, are key factors that promote transitions to dioecy and other forms of gender dimorphism.

  • Flowering plants have a wide range of mating patterns, from obligate outcrossing to predominant selfing. Selfing is commonly associated with the annual life form, and uncertain pollination conditions implicate reproductive assurance as the principal mechanism that drives the evolution of autonomous modes of selfing in plants.

  • Future work on plant sexual systems should abandon the myopic view of flowers as the sole reproductive unit and begin investigations into the functional interrelations between flowers, inflorescences and plant architecture, within the broader context of life-history evolution.

Abstract

Charles Darwin recognized that flowering plants have an unrivalled diversity of sexual systems. Determining the ecological and genetic factors that govern sexual diversification in plants is today a central problem in evolutionary biology. The integration of phylogenetic, ecological and population-genetic studies have provided new insights into the selective mechanisms that are responsible for major evolutionary transitions between reproductive modes.

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Figure 1: Floral design and pollen transfer in animal-pollinated plants.
Figure 2: The forms of enantiostyly in flowering plants.
Figure 3: Flexistyly in Alpinia (Zingiberaceae).
Figure 4: Intraspecific variation as a tool for studying the evolution and maintenance of monoecy and dioecy.
Figure 5: Multiple origins of predominant self-fertilization in flowering plants.
Figure 6: The difference in the distribution of outcrossing rates in animal-pollinated and wind-pollinated plant species.

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Acknowledgements

I thank W. Cole for assistance with figures; M. Dorken, C. Eckert, J. Heilbuth, L. Jesson and J. Willis for valuable discussion; and the Natural Sciences and Engineering Research Council of Canada for financial support.

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  1. Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, M5S 3B2, Ontario, Canada

    Spencer C. H. Barrett

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Glossary

SEXUAL POLYMORPHISM

The co-occurrence within a single interbreeding population of morphologically distinct mating groups that are distinguished by differences in their sexual organs.

DICHOGAMY

Differences in the timing of pollen dispersal from anthers and stigma receptivity of flowers. In protandry, pollen is dispersed before stigmas are receptive, and in protogyny, stigmas are receptive before pollen is dispersed from anthers.

INBREEDING DEPRESSION

The reduction in viability and fertility of inbred offspring compared with outbred offspring.

SUPERGENE CONTROL

A cluster of tightly linked co-adapted genes that are inherited as a single unit and carry out related functions.

ENANTIOSTYLY

Mirror-image flowers in which the style bends either to the left side or the right side of the floral axis. The phenomenon can exist as a sexual polymorphism with left-styled and right-styled plants.

MONOCOTYLEDON

(Monocot). One of the two classes of flowering plants, monocots are characterized by one embryonic leaf (cotyledon). Maize, rice and other grasses are common monocots.

RECIPROCAL HERKOGAMY

Sexual polymorphisms in which floral morphs differ reciprocally in the locations of female and male sex organs within flowers (for example, heterostyly and enantiostyly).

FLEXISTYLY

A sexual polymorphism in which populations contain two floral morphs that differ in the temporal patterns of style growth and orientation.

DIOECY

A sexual polymorphism in which populations contain female and male plants.

DISRUPTIVE SELECTION

Natural selection against the mean value of a quantitative trait, therefore favouring individuals at the two tails of the phenotypic distribution.

LIFE-HISTORY TRADE-OFF

When allocation of resources to one life-history trait reduces investment in another trait.

POLLEN DISCOUNTING

The loss of outcrossed siring success as a result of self-pollination.

ALLOZYME LOCI

Loci that code for different electrophoretic forms of the same enzyme as a result of allelic differences.

SEED DISCOUNTING

The formation of self-fertilized seeds from ovules that, if they had not been self-fertilized, would have been cross-fertilized.

COALESCENT ANALYSIS

A means of investigating the shared genealogical history of genes. A genealogy is constructed backwards in time starting with the present-day sample. Lineages coalesce when they have a common ancestor.

QUANTITATIVE TRAIT LOCI

(QTL). Loci that control quantitative traits identified by showing a statistical association between genetic markers and phenotypes that can be measured.

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Barrett, S. The evolution of plant sexual diversity. Nat Rev Genet 3, 274–284 (2002). https://doi.org/10.1038/nrg776

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