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

Abstract

Summary1. 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. 2. 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 latearriving 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. 3. 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. 4. 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.

An early gall-inducing parasitic wasp adversely affects the fitness of its host Ficus tree but not the pollinator

“…Although many studies 9 , 11 , 13 – 18 have shown that NPFWs can have a negative effect on the fig tree-fig pollinator mutulism due to the reduction in pollinator offspring or the seed production, some study has found that the NPFWs also can play a positive role in maintaining the stability of this obligate mutualism 32 . For example, parasites may stabilize and maintain the fig and fig wasp system through their effects on within- and between-tree reproductive phenology 32 . More specifically, oviposition by NPFWs can result in the asynchrony of the development of the figs, and increase the probabilities of pollinators finding oviposition sites, which is good for the maintenance of this mutualism 32 .…”

“…For example, parasites may stabilize and maintain the fig and fig wasp system through their effects on within- and between-tree reproductive phenology 32 . More specifically, oviposition by NPFWs can result in the asynchrony of the development of the figs, and increase the probabilities of pollinators finding oviposition sites, which is good for the maintenance of this mutualism 32 .…”

How to be a fig wasp parasite on the fig–fig wasp mutualism

“…Since all wasps leave the syconium more or less concurrently, early-ovipositing gallers have a longer pre-adult lifespan compared to those wasps, especially parasitoids, that oviposit later into the syconium. Early gallers accelerate the development time of the syconium presumably to pass quickly through larval stages vulnerable to parasitoids while late-arriving parasitoids retard syconium development, possibly to allow their offspring enough time to complete development [46]; successful parasitoid development at that late stage may also be facilitated by nutrition stored in their large eggs [28 ]. The mechanism by which syconium development time is influenced by syconium occupants is unknown.…”

“…The mechanism by which syconium development time is influenced by syconium occupants is unknown. Syconium ontogeny is likely a compromise between opposing selection pressures from gallers, parasitoids, and seeds [46].…”

Why resource history matters: age and oviposition history affect oviposition behaviour in exploiters of a mutualism

“…This fig species has served as an excellent model system for questions in evolutionary and functional ecology (e.g. Ghara et al ., ; Krishnan & Borges, ; Yadav & Borges, , ; Yadav et al ., ).…”