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A fundamental problem in ecology is to understand how mutualisms remain stable. The density-dependent regulations within interacting species potentially impact the persistence of these interspecific relationships. Yet few studies explore such intraspecific regulations’ role in stabilizing mutualisms. In addition, partner species often gain unequal benefits in mutualisms. To what extent such an interspecific asymmetry affects the stability of mutualisms is also poorly understood. We here developed a dynamic model for the asymmetric interaction between plants and their pollinators in nursery mutualisms, considering the intraspecific competition of each mutualist. We found that (i) a mutualism can be stabilized only if both mutualists are subject to the regulation of intraspecific competition; (ii) stabilizing the system also requires that the degree of asymmetry in benefits between mutualists must be limited to a range of ‘tolerance’, which narrows as intraspecific competition increases and even fades away with strong competition within both mutualistic species; (iii) when intraspecific competition within a species increases, the tolerant range is compressed from the side beneficial for it, with thus its partner species gaining relatively more benefit allocation; (iv) if the plant-pollinator interaction initiates from a small host plant population, these host plants must offer pollinators high levels of benefits, that can be subsequently reduced to favor plants once the mutualism has been successfully established. The agreement of empirical data to theoretical predictions suggests model reliability. These results highlight the role of intraspecific competition and the degree of benefit asymmetry between host plants and symbionts in stabilizing mutualisms.

In monoecious fig–wasp mutualisms (Ficus; ~350 spp.), tiny wasps obligately pollinate fig-tree inflorescences (‘figs’). Although pollination enables seed production, wasp symbionts also oviposit into flowers, replacing potential seeds with wasp offspring. Consistently across Ficus, ~40–60% of developed flowers produce seeds. Although several processes are probably involved, a general explanation for why wasps do not exploit more flowers has been elusive. However, interspecific scaling between host–symbiont reproductive traits suggests that as figs become larger across Ficus, the increase in wasp-eggs-per pollen-receptive fig will fail to match the increase in flower numbers. The potential for wasps to exploit hosts should thus decline due to an increasing excess of flowers. We tested these predictions, which were upheld, using data from 23 fig–wasp mutualisms from four continents. As fig size increases across Ficus, wasp egg-to-flower ratios, a measure of host–symbiont conflict of interest, declines, but the likelihood of a wasp egg successfully becoming an adult offspring increases. Host–symbiont conflict of interest thus varies systematically across Ficus due to variable relationships between key mutualist reproductive traits and fig size. We suggest that mutualism stability is more dependent upon mechanisms curtailing wasp flower exploitation in systems with small figs, and on preventing high foundress numbers in those with large figs.

The mutualism between the fig tree and the pollinating fig wasps is a keystone interaction in tropical forests. However, many antagonistic interactions also occur in the system, taking advantage of the fig trees and the pollinator. One such example is an antagonistic gall midge (Cecidomyiidae) that develops inside figs. Gall midges inside figs have been documented in a few Ficus species around the world, but to our knowledge they have not previously been observed in Panama. In this study the newly observed Panamanian fig gall midge is documented, together with its parasitoid wasp. The fig gall midge was only found in Ficus citrifolia figs. We investigated the effect of fig gall midge presence on the number of seeds and the number of pollinating wasps (Pegoscapus tonduzi) in a fig and aimed to identify the species based on morphology and barcoding of the COI region. We found that the fig gall midge had no, or a negligible effect, on the reproduction of the fig tree - fig wasp mutualism. The fig gall midge most likely belongs to the genus Ficiomyia, close to Ficiomyia perarticulata. The parasitoid belongs to the genus Physothorax, close to Physothorax russelli. This study suggests that the potentially newly arrived fig gall midge currently has no major effect on the fig tree - fig wasp mutualism. However, should infestation rates increase, it is likely that the fig gall midge would affect the mutualism negatively as it has in other parts of the world. More studies on the fig gall midge species distributions in this region would be valuable and would connect these newly observed species to a larger community, adding yet another species to this complex but classic example of a mutualism.

Insect herbivores can inflict substantial costs on plant reproductive success. Seed herbivory impacts directly by reducing the number of seeds and therefore the dispersal and reproductive potential of the plant. Fig trees, Ficus, provide keystone resources for tropical forests. The pollinating fig wasps develop inside figs, so consumption of unripe figs results in trees not only losing seeds but also their pollen dispersers. Selection to defend figs should therefore be strong. Seed herbivory is understudied in tropical forests and most data has been collected from fallen fruits. Here we use canopy sampling to identify fig-consuming larvae in central Panama and quantify both their consequences for the fig trees' reproductive success and the defensive value that ants provide against these larvae. Field surveys of 46 crops from nine fig species revealed that larvae could destroy up to 80% of figs on a tree. From seven Ficus species we barcoded (using COI) 51 individual fig consuming larvae (mainly Lepidoptera) that grouped into seven molecular operational taxonomic units. Lepidopteran larvae formed two feeding strategies, either stationary within a fig or tunneling between figs. Within the context of our study, stationary larvae were specialists whereas tunneling larvae were either specialists or generalists found on different Ficus species. Trees with ants had significantly fewer figs consumed by larvae (9% +/- 17% (mean +/- SD) for trees with azteca ants and 16% +/- 24% for trees with other ants) than did trees without ants (51% +/- 27%). Our results corroborate earlier findings that hosting ants can be an effective defensive mechanism for trees against seed herbivores or other antagonistic insects. Our study contributes to a wider body of research around the networks of insects associated with figs that highlights the importance of a multitrophic approach for understanding mutualism stability and persistence in the face of antagonism.

Active pollination has evolved four times in brood site pollination mutualisms. When pollination is active, the pollinator's behaviour specifically evolves to ensure flower fertilisation. In functionally dioecious Ficus species, the male figs host pollinating wasp larvae, while wasps cannot breed in the female figs because the styles are longer than the wasp ovipositor. Here we investigate the dioecious Ficus hispida. We show that in male figs, every time the wasp has laid an egg into a pistillate flower, it removes one pollen grain from its pollen pockets and places it on the hypopygium. When the wasp inserts its ovipositor into the next flower, the pollen grain is deposited deep within the style. Each ovipositor insertion results in flower pollination and insect oviposition. Because of systematic pollination of the flowers into which the eggs are laid, the wasp larvae benefit from feeding on fertilised endosperm while no seed are produced. In female figs, after probing a flower, the wasp presents pollination behaviour only every five visits. However, if it does occur, this behaviour lasts longer than in male figs and results in the deposition of on average 10 pollen grains on the hypopygium. The exposed sticky papillae on the stigmatic surface collect pollen from the hypopygium and pollen tubes may grow to neighbouring stigmas, ensuring secondary dispersal and efficient ovule fertilisation. Overall, our study demonstrates that the floral morphology of male figs facilitates precise pollen deposition, beneficial for the wasp progeny, while the floral morphology of female figs compensates for wasp pollination behaviour that is not selected in those figs. We conclude that the morphology of the arena in which interactions with its pollinator are played out is the result of selection on the plant to maximize its male and female fitness. Incidentally, this morphology stabilises the mutualistic interaction.

Obligate pollination mutualisms, in which plant and pollinator lineages depend on each other for reproduction, often exhibit high levels of species specificity. However, cases in which two or more pollinator species share a single host species (host sharing), or two or more host species share a single pollinator species (pollinator sharing), are known to occur in current ecological time. Further, evidence for host switching in evolutionary time is increasingly being recognized in these systems. The degree to which departures from strict specificity differentially affect the potential for hybridization and introgression in the associated host or pollinator is unclear. We addressed this question using genome-wide sequence data from five sympatric Panamanian free-standing fig species (Ficus subgenus Pharmacosycea, section Pharmacosycea) and their six associated fig–pollinator wasp species (Tetrapus). Two of the five fig species, F. glabrata and F. maxima, were found to regularly share pollinators. In these species, ongoing hybridization was demonstrated by the detection of several first-generation (F1) hybrid individuals, and historical introgression was indicated by phylogenetic network analysis. By contrast, although two of the pollinator species regularly share hosts, all six species were genetically distinct and deeply divergent, with no evidence for either hybridization or introgression. This pattern is consistent with results from other obligate pollination mutualisms, suggesting that, in contrast to their host plants, pollinators appear to be reproductively isolated, even when different species of pollinators mate in shared hosts.

Changes in habitat have led to a decline in many species which are now threatened. One of them is the spring pasque flower Pulsatilla vernalis, which grows on well-drained soils and is sensitive to competition. The species has in the past benefited from disturbances such as grazing, mowing and forest fires. Now that these do not occur as frequently, it has been suggested that prescribed burning could be used as a conservation intervention to benefit P. vernalis. In this study, we tested whether prescribed burning in 2018 benefited a population of P. vernalis at Marma military training area, outside Älvkarleby in eastern Sweden. Due to unexpected windy conditions on the day of the prescribed burning, not all the planned area was burned. This created a natural experiment that enabled us to compare burned areas with unburned areas (control) in both heathland and forested heathland habitats. The study includes data gathered before and after the experimental treatment. We found that compared to the control areas, the burned areas had a significantly higher number of P. vernalis tufts (clusters of leaf rosettes), as well as a greater number of flower stalks per tuft. Although limited due to lack of replication, this study supports the suggestion that prescribed burning benefits P. vernalis, both in open areas as well as in forests. 

Pollinating insects are decreasing worldwide in abundance, biomass, and species richness, affecting the plants that rely on pollinators for fruit production and seed set. Insects are often sensitive to high temperatures. The projected temperature increases may therefore severely affect plants that rely on insect pollinators. Highly specialized mutualisms are expected to be particularly vulnerable to change because they have fewer partner options should one partner become unavailable. In the highly specialized mutualism between fig trees and their pollinating fig wasp, each fig species is pollinated by only one or a few wasp species. Because of their year-round fruit production, fig trees are considered a keystone resource for tropical forests. However, to produce fruits, wild fig trees need to be pollinated by fig wasps that typically travel a long one-way trip from the tree donating pollen to the tree receiving pollen. In a few previous studies from China and Australia, increasing temperatures dramatically decreased fig wasp lifespan. Are these grim results generalizable to fig mutualisms globally? Here, we use survival experiments to determine the effect of increasing temperature on the lifespan of Neotropical fig wasps associated with five common Panamanian Ficus species. Experimental temperatures were based on the current daytime mean temperature of 26.8 degrees C (2SD: 21.6-31.7 degrees C) and the predicted local temperature increase of 1-4 degrees C by the end of the 21st century. We found that all tested pollinator wasp species had a significantly shorter lifespan in 30, 32, 34, and 36 degrees C compared to the current diurnal mean temperature of 26 degrees C. At 36 degrees C pollinator median lifespan decreased to merely 2-10 h (6%-19% of their median lifespan at 26 degrees C). Unless wasps can adapt, such a dramatic reduction in lifespan is expected to reduce the number of pollinators that successfully disperse to flowering fig trees, and may therefore jeopardize both fruit set and eventually survival of the mutualism.

Mutualisms are of fundamental ecological importance, but risk breaking down if one partner stops paying the costs yet still takes the benefits of the interaction. To prevent such cheating, many mutualisms have mechanisms that lower the fitness of uncooperative symbionts, often termed host sanctions. In mutualisms where the interacting partners are species-specific, we would expect to see coevolution of the levels of host sanctions and partner cooperation across species-pairs. In the mutualism between fig trees and their species-specific pollinating fig wasps, host sanctions vary greatly in strength, and wasp cooperation levels vary accordingly. Here I show experimentally that in Panamanian Ficus perforata (section Urostigma, Americana) there are fitness costs for wasps that do not pollinate. These fitness costs are caused by a combination of abortions of unpollinated figs and reduced proportion of wasp larvae that successfully develop to adults. The relative fitness of wasps that do not pollinate compared to wasps that pollinate is 0.59, leading to the intermediate sanction strength 0.41. Next, by screening pollinators of F. perforata I found that 1.9% of wasp individuals in natural populations failed to carry pollen. Across five actively pollinated Neotropical fig species and their pollinators, fig species with stronger host sanctions had fewer uncooperative wasps, as would be expected if sanctions promote cooperation.

Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory's relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a "cheater" that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.