Different rewards in female and male flowers can explain the evolution of sexual dimorphism in plants

Abstract

Insects use floral signals to find rewards in flowers, transferring pollen in the process. In unisexual plants, the general view is that staminate (male) and pistillate (female) flowers obtain conspecific pollen transfers by advertising their rewards with similar floral signals. For female plants lacking food rewards, this can lead to floral mimicry and pollination by deceit. In this study, we challenge this view by presenting evidence for different rewards offered by flowers on females and males, as a mechanism promoting sexual dimorphism in Leucadendron xanthoconus (Proteaceae), a clearly sexually dimorphic shrub. The tiny beetle pollinators Pria cinerascens (Nitidulidae) depend entirely on the plants they pollinate for survival and reproduction. Male flowers provide mating and egglaying sites, and food for adults and larvae. Female flowers lack nectar and function to shelter pollinators from rain. Their flower heads have cup-shaped display leaves, and are more closed than are those in males. On rainy days, flowers on females received 30% more visits than did flowers on males, and 90% more than they did on sunny days. When we removed display leaves in females, intact flower heads received 14 times more P. cinerascens visits than did manipulated flower heads, indicating that the cup shape attracts the beetles. In both sexes, having many flowers increased the probability of visits and the number of P. cinerascens visiting a plant. In males, the number of larvae was positively correlated with floral-display size, while in females, seed set (pollen transfers) showed no relationship with floral-display size. Ninety-five per cent of the ovules received pollen and 52% matured into seeds. We explain the sexual dimorphism in L. xanthoconus as a result of an intimate partnership with P. cinerascens pollinators, in conjunction with a rainy climate. Pollinators favour large male floral displays, because they offer a reliable food source for adults and larvae. Frequent rains drive the P. cinerascens to leave males in search of the protection offered by females. Because females offer shelter, an essential resource that is not offered by male plants, they receive sufficient pollen independent of their floral-display size. This pollination system promotes the evolution of sexually dimorphic floral signals, guiding pollinators to different rewards in male and female flowers.

Experimental Evaluation of Insect Pollination versus Wind Pollination in Leucadendron (Proteaceae)

“…However, female inflorescences appear to offer no floral rewards to P. cinerascens. Hemborg and Bond (2005) thought that P. cinerascens were attracted to female L. xanthoconus inflorescences because they offered shelter, an essential resource not offered by male inflorescences. Our observations support this, in that the beetles hide between the inflorescence and the surrounding leaves.…”

“…A small pollen beetle, Pria cinerascens Er. (Nitidulidae), is often associated with Leucadendron flowers, particularly the male inflorescences, where they feed on pollen and breed (Williams 1972;Hattingh and Giliomee 1989;Hemborg and Bond 2005). Williams (1972) suggested that at least six species are wind pollinated because of morphological changes such as a lack of conspicuous colored involucral leaves, a reduction of the hypogynous scale (nectaries), increased size of the female stigmatic surface, a lack of distinct floral odor, and showering of pollen when branches are shaken.…”

Differences in the diversity and composition of the pollinator assemblage of two co-flowering congeneric alpine wallflowers, Erysimum nevadense and E. baeticum

“…Pollination by beetles has been shown in a number of plants, most times in highly specialized relationships (Anstett, 1999;Franz, 2007;Gibernau et al, 1999;Hemborg and Bond, 2005;Ratnayake et al, 2006;Terry et al, 2005;Woitke et al, 2006). Nevertheless, generalist plants mostly pollinated by beetles have been also reported (Daphne laureola, Alonso, 2004;Romulea spp., Goldblatt et al, 2002;Shorea parviflora, Sakai et al, 1999).…”

Canopy seed storage is associated with sexual dimorphism in the woody dioecious genus Leucadendron

“…Similarly, while many species of Leucadendron release their seeds from their ‘cones’ when they are mature, many others are strongly serotinous and maintain their seed bank in cones for several years before their release (Williams 1972). The causes of the often extreme sexual dimorphism displayed by some Leucadendron species has attracted a good deal of attention (Bond & Midgley 1988; Bond & Maze 1999; Hemborg & Bond 2005), but the possibility of an association between sexual dimorphism and serotiny, and its potential implications, has never been investigated.…”

“…Although little is known about the details of pollination in Leucadendron , some species are wind‐pollinated, while others are pollinated by insects (Rebelo 2001). Bond & Maze (1999) and Hemborg & Bond (2005) showed that pollinator visitation increased with ramification in males of L. xanthoconus , putatively because highly ramified males had more showy inflorescence displays (Bond & Midgley 1988). If selection on traits that influence siring success has contributed to the evolution of sexual dimorphism in Leucadendron , as these studies suggest, then one might expect an association between dimorphism and the pollination mode.…”