Jo Ridley

A role for parasites in stabilising the fig-pollinator mutualism

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.

Interference competition and high temperatures reduce the virulence of fig wasps and stabilize a fig-wasp mutualism.

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.

Oviposition strategies, host coercion and the stable exploitation of figs by wasps

A classic example of a mutualism is the one between fig plants (Ficus) and their specialized and obligate pollinating wasps. The wasps deposit eggs in fig ovules, which the larvae then consume. Because the wasps derive their fitness only from consumed seeds, this mutualism can persist only if the wasps are prevented from laying eggs in all ovules. The search for mechanisms that can limit oviposition and stabilize the wasp–seed conflict has spanned more than three decades. We use a simple foraging model, parameterized with data from two Ficus species, to show how fig morphology reduces oviposition rates and helps to resolve the wasp–seed conflict. We also propose additional mechanisms, based on known aspects of fig biology, which can prevent even large numbers of wasps from ovipositing in all ovules. It has been suggested that in mutualistic symbioses, the partner that controls the physical resources, in this case Ficus, ultimately controls the rate at which hosts are converted to visitors, regardless of relative evolutionary rates. Our approach provides a mechanistic implementation of this idea, with potential applications to other mutualisms and to theories of virulence.

Kin competition within groups: the offspring depreciation hypothesis

Where relatives compete for the same resources (kin competition) and each obtains an equal share, this can favour the evolution of elevated dispersal rates, such that most resource competition is among non–relatives. We show that this effect evaporates as among–sibling dominance increases to the point where the allocation of resources is maximally unequal. We restore a kin–competition effect on emigration rates from dominance–ranked family groups by showing that where siblings form queues to inherit the breeding positions, the length of the queue affects the fitness of all individuals by depreciating the rank of subsequent offspring. Incorporating this ‘offspring depreciation’ effect decreases optimal queue lengths, increases dispersal rates and explains the otherwise paradoxical use of sinks by cooperatively breeding birds in stable environments. The offspring depreciation effect also favours the evolution of small, but consistent, clutch sizes and high reproductive skew, but constrains the evolution of alloparenting.

Population regulation in group-living birds: predictive models of the Seychelles warbler

A major challenge for population ecology is to predict population responses to novel conditions, such as habitat loss. This frequently involves understanding dispersal decisions, in terms of their consequences for fitness. However, this approach requires detailed data, and is thus often inappropriate for urgent problems on poorly known species. This may be resolved by developing a predictive framework based on well-studied species, for applying to those that are less well understood. Population size, group sizes and habitat occupancy of the Seychelles warbler (Acrocephalus sechellensis) can be predicted by determining the evolutionary stable dispersal strategy. For densities near to demographic equilibrium, regulation results from the combined effects of non-breeding and use of sink habitats. In the Seychelles warbler, resident male non-breeders compete for breeding vacancies on neighbouring territories. The resulting kin competition is a key process for predicting the observed balance between regulation by non-breeding and regulation by sink use. Family groups, in which offspring delay dispersal, hoping to fill a vacancy on a local territory, are common among group-living species. This suggests that kin competition may frequently play a central role in the population regulation of socially complex species. Although all the model variants considered are complex, predictions are shown to be insensitive to a range of simplifications, illustrating that, despite significant evolutionary import at the individual level, some behaviour can be unimportant when considering population level questions. Identifying which behavioural strategies have significant demographic consequences is key to the further development of population models based on fitness maximizing behaviour.