Active pollination in a functionally dioecious Ficus species: An interplay between pollinator behaviour and floral morphology

Abstract

Active pollination has evolved four times in brood site pollination mutualisms. When pollination is active, the pollinator's behaviour specifically evolves to ensure flower fertilisation. In functionally dioecious Ficus species, the male figs host pollinating wasp larvae, while wasps cannot breed in the female figs because the styles are longer than the wasp ovipositor. Here we investigate the dioecious Ficus hispida. We show that in male figs, every time the wasp has laid an egg into a pistillate flower, it removes one pollen grain from its pollen pockets and places it on the hypopygium. When the wasp inserts its ovipositor into the next flower, the pollen grain is deposited deep within the style. Each ovipositor insertion results in flower pollination and insect oviposition. Because of systematic pollination of the flowers into which the eggs are laid, the wasp larvae benefit from feeding on fertilised endosperm while no seed are produced. In female figs, after probing a flower, the wasp presents pollination behaviour only every five visits. However, if it does occur, this behaviour lasts longer than in male figs and results in the deposition of on average 10 pollen grains on the hypopygium. The exposed sticky papillae on the stigmatic surface collect pollen from the hypopygium and pollen tubes may grow to neighbouring stigmas, ensuring secondary dispersal and efficient ovule fertilisation. Overall, our study demonstrates that the floral morphology of male figs facilitates precise pollen deposition, beneficial for the wasp progeny, while the floral morphology of female figs compensates for wasp pollination behaviour that is not selected in those figs. We conclude that the morphology of the arena in which interactions with its pollinator are played out is the result of selection on the plant to maximize its male and female fitness. Incidentally, this morphology stabilises the mutualistic interaction.