A Role for Parasites in Stabilising the Fig-Pollinator Mutualism

Abstract

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their “fruits” (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism

“…We show that when followed by nonsterilizing species later in ontogeny, these putative parasites can confer complementary benefits to plants. In other mutualisms, parasites have been shown to strengthen the relationship between mutualistic species (47,48); in contrast, our results suggest that, in some cases, the persistent language of "mutualists" vs. "free-loaders" or "cheaters" may be misleading.…”

Composition and structure of the fig wasp community in Amazonia

“…For this to occur, it is necessary that the figs have at least some similar morphological characteristics. Phenoptic diversity with respect to syconium size indirectly causes the restriction of a considerable number of non-pollinating wasps, since large figs have a thicker receptacle wall which does not allow some species to reach the flower ovules during oviposition (Dunn et al 2008).…”

Spatial Stratification of Internally and Externally Non-Pollinating Fig Wasps and Their Effects on Pollinator and Seed Abundance in Ficus burkei

“…Female pollinating wasps (foundresses) lay their eggs by inserting their ovipositors down the flower styles. At maturation, wasp galls are clustered at the syconium's centre [4,6,[9][10][11][12][13] with seeds at the outer wall. This spatial stratification of pollinating wasps and seeds enables mutualism stability, although the mechanisms preventing the wasps from galling all ovules are unclear.…”

“…[12]) or biased offspring survival (e.g. [13][14][15]). Ovipositing foundress wasps may favour inner ovules because of shorter handling times offered by the short styles [10,12].…”

“…Ovipositing foundress wasps may favour inner ovules because of shorter handling times offered by the short styles [10,12]. Interference competition between foundresses, which further slows oviposition [16], and limited longevity [13,16] means that wasps die before all ovules are galled. Like most mutualisms [17,18], the fig-pollinator system is exploited by third parties, which mainly consist of nonpollinating fig wasps (NPFWs) that attack with their long ovipositors from outside of the syconium and, depending on the species, exert costs onto either mutualist by parasitism or seed predation.…”