Parasites and investment to host inflorescences in a fig tree–fig wasp mutualism

Abstract

Most mutualisms are parasitized by third-party species that inflict costs to the mutualists. How such parasites affect mechanisms that help maintain mutualism stability is poorly understood, even in well-studied systems. Angiosperm plants tend to invest most resources in tissue that yields high net benefits. In mutualisms with plant hosts, reduction in such investment can function as a key stability-promoting mechanism, such as in fig–wasp mutualisms. Here, uncooperative symbiont wasps that fail to pollinate incur “sanctions” via reduced host investment to unpollinated figs, realized via fig abortion, killing all wasp offspring, or via elevated offspring mortality within unaborted figs. We experimentally exposed host Ficus racemosa figs to parasitic wasps Sycophaga fusca, which convert fig flowers into offspring without benefitting host trees, with or without uncooperative (pollen-free) or cooperative (pollen-laden) symbiont pollinator wasps Ceratosolen fusciceps. Pollen-free C. fusciceps were still able to convert fig flower ovaries into wasp offspring, whereas those naturally pollen laden were prevented from reproducing by experimental manipulation. Independent of the effects of pollination and reproduction by pollinators, increased exposure to S. fusca parasites resulted in reduced rates of fig abortion and gall failure in unaborted figs. Although S. fusca convert flower ovaries that could otherwise become beneficial pollinator offspring or fig seeds into parasite offspring, figs with intermediate levels of parasite exposure received high levels of investment. Our results suggest that S. fusca parasite oviposition/larval activities can result in host trees boosting investment to figs, even when this may counter the tree's interests. We suggest that oviposition/larval activity by these parasites may mimic the biochemical pathways of pollinator gall formation and seed production.