Interference Competition and High Temperatures Reduce the Virulence of Fig Wasps and Stabilize a Fig-Wasp Mutualism

Abstract

Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia (‘figs’) that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can ‘set the rules of the game’ to ensure mutualistic behavior in its symbionts.

Spatial heterogeneity and host repression in fig-fig wasp mutualism

“…Table 2 shows that fruit size, number of vacant female flowers, total female flowers and foundress number are correlated significantly with the production of viable seeds and wasp galls for some crops but not for others. Foundress number per syconium also increased with fruit size (N=93, (Figure 4, also see [29]). The quick closure of osiole will prevent the extra more pollinator wasps from entering the syconium cavities and/or from exiting the syconium cavities after pollinators entering lumen, which will create the intensive interference competition among the foundresses in their egg preposition [16].…”

“…This can preclude the breakdown of cooperation between figs and fig wasps [44,49]. A controlled experiment shows that figs close their ostiole rapidly if many foundresses enter a syconium but keep it open when foundress numbers are low [29]. This suggests that figs detect and respond to foundress numbers, preventing the presence of too many foundresses in the syconia and thereby the conflict between the figs and fig wasps rather than relying on intrinsic features of the figs or evolutionary-restraint of the pollinators.…”

“…The pollinator wasps enter the central lumen of the receptive fruits through the ostiole consistence of bracts, and the fig will enclose the ostiole properly after the pollinator wasps entering the syconium cavity, and our previous experiment showed that the ostiole closure will be a density dependent process as a function of foundress number [29]. In these experiments, we will examine whether the ostiole closure of fig will differ between seasons.…”

“…The pollination and oviposition efficiency of foundresses might greatly affect the trade-off between the figs and pollinators wasps [22,28,29]. We also examined whether the pollination and oviposition efficiency of foundresses varies seasonally.…”

“…Such one wasp examination on whether the ostioles are enclosed was carried every 4 h in the time that ostioles have not begun to enclose, but was carried every 1 h when the ostioles begin to enclose. This rough estimation on how long the ostiole will be enclosed after the foundress is introduced into the fig cavity is based on the previous observation or experiment results [29].…”