Active pollination favours sexual dimorphism in floral scent

Abstract

Zoophilous flowers often transmit olfactory signals to attract pollinators. In plants with unisexual flowers, such signals are usually similar between the sexes because attraction of the same animal to both male and female flowers is essential for conspecific pollen transfer. Here, we present a remarkable example of sexual dimorphism in floral signal observed in reproductively highly specialized clades of the tribe Phyllantheae (Phyllanthaceae). These plants are pollinated by species-specific, seed-parasitic Epicephala moths (Gracillariidae) that actively collect pollen from male flowers and pollinate the female flowers in which they oviposit; by doing so, they ensure seeds for their offspring. We found that Epicephala-pollinated Phyllanthaceae plants consistently exhibit major qualitative differences in scent between male and female flowers, often involving compounds derived from different biosynthetic pathways. In a choice test, mated female Epicephala moths preferred the scent of male flowers over that of female flowers, suggesting that male floral scent elicits pollen-collecting behaviour. Epicephala pollination evolved multiple times in Phyllantheae, at least thrice accompanied by transition from sexual monomorphism to dimorphism in floral scent. This is the first example in which sexually dimorphic floral scent has evolved to signal an alternative reward provided by each sex, provoking the pollinator's legitimate altruistic behaviour.

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

“…Proximately, both pre‐ and postoviposition barriers may mediate this specificity. There is evidence not only that host‐recognition cues such as floral odor may mediate specificity in leafflowers (Okamoto et al, 2007, 2013), but also that larvae may suffer reduced survivorship on the “wrong” hosts in yuccas and figs (Smith et al, 2009; Moe et al, 2011; Cornille et al, 2011; see Althoff, 2016, in this issue) suggesting that the antagonistic seed‐eating part of the interaction may in part be responsible for this specificity. In the case of figs, host specialization may be proximately due to the ability to successfully initiate galls on fig flowers (Ghana et al, 2015).…”

A Novel, Enigmatic Basal Leafflower Moth Lineage Pollinating a Derived Leafflower Host Illustrates the Dynamics of Host Shifts, Partner Replacement, and Apparent Coadaptation in Intimate Mutualisms

“…and Epicephala. For instance, floral odor blends emitted by leafflowers are known to vary both among species within a clade (Okamoto et al 2007) as well as among clades (Okamoto et al 2013), and these blends are responsible for mediating host recognition by female moths. More derived Epicephala females possess a sclerotized ovipositor, which is used in most cases for laying eggs inside ovary tissue of leafflower flowers rather than on the external surface of the carpels (Kawakita and Kato 2009, 2016; but see Zhang et al 2012 b ).…”

“…The 300 species of Glochidion and their presumably similar number of Epicephala species are widely distributed in east, south, and southeast Asia, Australia, New Guinea, and the Pacific Islands and have received concerted attention from multiple groups of investigators, particularly in East Asia and Polynesia (Kato et al 2003; Kawakita and Kato 2006, 2016; Okamoto et al 2007,2013; Goto et al 2010; Hembry et al 2012,2013; Zhang et al 2012 a ; Mochizuki et al 2014; Okamoto 2014; Li et al 2015). In East Asia, Glochidion and their Epicephala show very high species specificity (Kawakita and Kato 2006, 2016; Zhang et al 2012 a ; Li et al 2015), which is mediated by species-specific floral odor blends (Okamoto et al 2007, 2013). Epicephala females actively pollinate Glochidion flowers, inserting pollen into the recessed stigmatic surface and ovipositing inside the locules of the flowers’ ovaries.…”

Characterization ofSalix nigrafloral insect community and activity of three nativeAndrenabees

“…Our results are unusual given that dioecious plants, in which both sexes offer rewards, are often dimorphic in both scent composition and emission levels (Füssel 2007; Ashman 2009; Okamoto et al 2013). Nevertheless, this pattern does not always hold true in the Salix genus.…”