Darwin's legacy: the forms, function and sexual diversity of flowers

Abstract

Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwin's insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwin's seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwin's efforts towards integration.

Figure 1.

Examples of species that exhibit the six reported stylar polymorphisms in flowering plants: (a) distyly—Primula beesiana (Primulaceae); (b) tristyly—Eichhornia azurea (Pontederiaceae); (c) stigma-height dimorphism—Narcissus gaditanus (Amaryllidaceae); (d) enantiostyly—Wachendorfia paniculata (Haemodoraceae); (e) flexistyly—Alpinia mutica (Zingiberaceae); (f) inversostyly—Hemimeris racemosa (Scrophulariaceae), image courtesy of Anton Pauw. General features of these polymorphisms are summarized in table 2.

Figure 2.

Enantiostyly promotes cross-pollination and reduces the incidence of self-fertilization in Solanum rostratum (Solanaceae). Outcrossing rates, estimated using allozyme markers, were compared in experimental arrays exhibiting three contrasting stylar conditions: plants with straight styles, plants with mixtures of right- and left-handed styles (monomorphic enantiostyly) and plants with either right- or left-handed styles (dimorphic enantiostyly). The pie diagram illustrates the proportion of matings in dimorphic enantiostylous arrays that resulted from self-fertilization (white), outcrossing between plants of the same style orientation (cross-hatched) and outcrossing between plants of opposite stylar orientation (black). After Jesson & Barrett (2002c), figure published with permission from Nature.

Figure 3.

Examples of species that exhibit heteranthery: (a) Cassia fistula (Caesalpinioideae) being visited by a Carpenter bee (Xylocopa spp.). FA indicates the feeding anthers and PA the pollinating anthers; (b) Solanum citrullifolium (Solanaceae), image courtesy of Mario Vallejo-Marín; (c) Heteranthera multiflora (Pontederiaceae) exhibits dimorphic enantiostyly, a left-handed flower is illustrated (see §3c); (d) Cyanella alba (Tecophilaeaceae) is reported to be dimorphically enantiostylous, a left-handed flower is illustrated. Image courtesy of Lawrence Harder.

Figure 4.

The diversity of sexual systems that can potentially occur in a species with three sex phenotypes: hermaphrodite, female and male. (a) Location of the five sexual systems resulting from plotting population sex ratios into a triangle of sex phenotype space. (b) The observed pattern of sex-ratio variation in a sample of 116 populations of the clonal aquatic Sagittaria latifolia from the northern portion of its range in eastern N. America. Each black dot represents a single population and is located on the triangle based on the frequencies of sex phenotypes within each population. Dots within the triangle are populations that contain all three phenotypes, populations with two sex phenotypes are on the axes, and populations containing a single sex phenotype are located on the apices of the triangle. Sampling of flowering ramets in each population followed methods detailed in Dorken & Barrett (2004b). Unpublished data of S. B. Yakimowsi & S. C. H. Barrett (2009).