The evolution of parasitism from mutualism in wasps pollinating the fig, Ficus microcarpa, in Yunnan Province, China.

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.

Sulfadiazine Masquerading as a Natural Product from Scilla madeirensis (Scilloideae).

The structure of 2,4-(4'-aminobenzenamine)pyrimidine (1), a pyrimidine alkaloid previously isolated from the bulbs of Scilla madeirensis (Asparagaceae, synonym Autonoë madeirensis), has been revised. These conclusions were met via comparison of reported NMR and EIMS data with those obtained from synthetic standards. The corrected structure is the antibiotic sulfadiazine (2), which has likely been isolated as a contaminant from the site of collection. The reported bioactivity of 1 as an α1-adrenoceptor antagonist should instead be ascribed to sulfadiazine. Our findings appear to show another example of an anthropogenic contaminant being identified as a natural product and emphasize the importance of considering the biosynthetic origins of isolated compounds within a phylogenetic context.

Why mutualist partners vary in quality: mutation-selection balance and incentives to cheat in the fig tree-fig wasp mutualism.

Mutualisms between species are ecologically ubiquitous but evolutionarily puzzling. Host discrimination mechanisms that reduce the fitness of uncooperative symbionts can stabilise mutualism against collapse, but also present a paradox - if discrimination is effective, why do uncooperative symbionts persist? Here, we test whether mutations or fitness benefits of cheating best explain the prevalence of uncooperative wasps in the fig tree-fig wasp mutualism. By combining theory with field-collected data we demonstrate that the proportions of pollen-free wasps of strongly discriminating hosts are reached with reasonable mutation rates. In contrast, in weakly discriminating hosts, the required mutation rates, assuming a single locus, are untenably high, but the required cheater advantages fall within expected ranges. We propose that when discrimination is weak, uncooperative symbionts proliferate until they reach the equilibrium proportion that balances costs and benefits of cheating. Our results suggest that mechanisms that resolve the paradox of uncooperative symbionts differ among host species.

Host sanctions in Panamanian Ficus are likely based on selective resource allocation.

PREMISE OF THE STUDY: Fig trees and their pollinators, fig wasps, present a powerful model system for studying mutualism stability: both partners depend on each other for reproduction, cooperation levels can be manipulated, and the resulting field-based fitness quantified. Previous work has shown that fig trees can severely reduce the fitness of wasps that do not pollinate by aborting unpollinated figs or reducing the number and size of wasp offspring. Here we evaluated four hypotheses regarding the mechanism of sanctions in four Panamanian fig species. METHODS: We examined wasp and fig samples from field experiments with manipulated levels of pollination. KEY RESULTS: In unpollinated figs, the fig wall and the wasp offspring had a lower dry mass. Unpollinated figs had as many initiated wasp galls as pollinated figs but fewer galls that successfully produced live wasp offspring. Across three experimentally increasing levels of pollination, we found nonlinear increases in fig wall mass, the proportion of wasp galls that develop, and wasp mass. CONCLUSIONS: Our data did not support the hypotheses that lack of pollination prevents gall formation or that fertilized endosperm is required for wasp development. While our data are potentially consistent with the hypothesis that trees produce a wasp-specific toxin in response to lack of pollination, we found the hypothesis that sanctions are a consequence of trees allocating more resources to better-pollinated figs more parsimonious with the aggregate data. Our findings are completely analogous to the selective resource allocation to more beneficial tissues documented in other mutualistic systems.

Pollinator and host sharing lead to hybridization and introgression in Panamanian free-standing figs, but not in their pollinator wasps.

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.

Rising temperatures threaten pollinators of fig trees-Keystone resources of tropical 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°C (2SD: 21.6-31.7°C) and the predicted local temperature increase of 1-4°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°C compared to the current diurnal mean temperature of 26°C. At 36°C pollinator median lifespan decreased to merely 2-10 h (6%-19% of their median lifespan at 26°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.

Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism.

Theory predicts that mutualisms should be vulnerable to invasion by cheaters, yet mutualistic interactions are both ancient and diverse. What prevents one partner from reaping the benefits of the interaction without paying the costs? Using field experiments and observations, we examined factors affecting mutualism stability in six fig tree-fig wasp species pairs. We experimentally compared the fitness of wasps that did or did not perform their most basic mutualistic service, pollination. We found host sanctions that reduced the fitness of non-pollinating wasps in all derived, actively pollinated fig species (where wasps expend time and energy pollinating), but not in the basal, passively pollinated fig species (where wasps do not). We further screened natural populations of pollinators for wasp individuals that did not carry pollen ('cheaters'). Pollen-free wasps occurred only in actively pollinating wasp species, and their prevalence was negatively correlated with the sanction strength of their host species. Combined with previous studies, our findings suggest that (i) mutualisms can show coevolutionary dynamics analogous to those of 'arms races' in overtly antagonistic interactions; (ii) sanctions are critical for long-term mutualism stability when providing benefits to a host is costly, and (iii) there are general principles that help maintain cooperation both within and among species.

Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps.

The fig and pollinator wasp obligate mutualism is diverse (∼750 described species), ecologically important, and ancient (∼80 Ma). Once thought to be an example of strict one-to-one cospeciation, current thinking suggests genera of pollinator wasps codiversify with corresponding sections of figs, but the degree to which cospeciation or other processes contribute to the association at finer scales is unclear. Here, we use genome-wide sequence data from a community of Panamanian strangler figs and associated wasp pollinators to estimate the relative contributions of four evolutionary processes generating cophylogenetic patterns in this mutualism: cospeciation, host switching, pollinator speciation, and pollinator extinction. Using a model-based approach adapted from the study of gene family evolution, our results demonstrate the importance of host switching of pollinator wasps at this fine phylogenetic and regional scale. Although we estimate a modest amount of cospeciation, simulations reveal the number of putative cospeciation events to be consistent with what would be expected by chance. Additionally, model selection tests identify host switching as a critical parameter for explaining cophylogenetic patterns in this system. Our study demonstrates a promising approach through which the history of evolutionary association between interacting lineages can be rigorously modeled and tested in a probabilistic phylogenetic framework.

Selective resource allocation may promote a sex ratio in pollinator fig wasps more beneficial for the host tree.

Mutualisms play a key role in most ecosystems, yet the mechanisms that prevent overexploitation of the mutualistic relationship are still poorly understood. In the mutualism between fig trees and their pollinating wasps both partners depend on each other. Fig trees benefit from female wasps that disperse their pollen, whereas wasps frequently benefit from a higher ratio of male offspring. Here we use manipulative field experiments to address whether host trees (Ficus racemosa) can influence the offspring sex ratio of the pollinator wasp. We controlled wasp matings; virgin wasps can lay only male eggs. We found that virgin foundress wasps had fewer offspring than mated foundresses. This was not caused by virgin wasps having a shorter lifespan, or laying fewer eggs. Instead, male wasp larvae were more likely to die during development. Additionally, male eggs were deposited in flowers of equal style length to those of female eggs, yet emerged from galls with shorter pedicels than those of female wasps. We suggest that male larvae are either allocated less resources by the tree, or are less able to attract resources, during development. If the tree orchestrates this difference it would promote a more female-biased wasp brood, thus increasing the tree's fitness.