Parasites exert conflicting selection pressures to affect reproductive asynchrony of their host plant in an obligate pollination mutualism

Plant reproductive phenology is generally viewed as an individual's strategy to maximize gamete exchange and propagule dispersal and is often considered largely dependent on patterns of floral initiation. Reproductive phenology, however, can be affected by proximate responses to pollinators, parasites and herbivores which could influence floral longevity or fruit development time. We examined the influence of insect interactants on within‐plant reproductive phenology in the fig–fig wasp nursery pollination mutualism in Ficus racemosa (Moraceae). Most figs support a wasp community comprised of a mutualistic pollinator, with several host‐plant‐specific non‐pollinating herbivorous gallers and parasitoids. These wasps reproduce within enclosed inflorescences called syconia, which develop into fruit after pollination. While different wasp species oviposit into syconia at varying times during its ontogeny, all wasp progeny are constrained to exit syconia simultaneously just prior to fruit ripening. Developing larvae of early‐ovipositing wasps may hasten syconium ontogeny through formation of earlier and larger nutrient sinks, whereas larvae of late‐arriving parasites may lengthen syconium ontogeny to complete their development successfully. Seeds are also important nutrient sinks. The number of seeds and the type and number of developing wasps may therefore be expected to influence syconium development times, thereby affecting the reproductive synchrony of syconia on a plant. Observations on naturally pollinated and parasitized syconia indicated that their seed and wasp content affected syconium development time. Experimental manipulations of syconia to produce only seeds or various combinations of wasps confirmed this finding. Early‐ovipositing galler progeny reduced syconium development times, while gallers ovipositing concurrently with pollinators had no effect on syconium development. Late‐ovipositing parasitoid progeny, the presence of only seeds within the syconium, or delayed pollination increased syconium development time. The differential development of syconia, which was influenced by mutualistic or parasitic progeny, accordingly contributed to within‐tree reproductive asynchrony. Synthesis. Individual reproductive units in fig trees called syconia, which also function as brood sites for pollinating and parasitic fig wasps, have plastic development durations dependent on pollination timing and species of wasps developing within them. Syconium development times are a likely compromise between conflicting demands from developing seeds and different wasp species.