Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites

Figs (Ficus spp., Moraceae) and their pollinating wasps form an obligate mutualism, which has long been considered a classic case of coevolution and cospeciation. Figs are also exploited by several clades of nonpollinating wasps, which are parasites of the mutualism and whose patterns of speciation have received little attention. We used data from nuclear and mitochondrial DNA regions to estimate the phylogenies of 20 species of Pleistodontes pollinating wasps and 16 species of Sycoscapter nonpollinating wasps associated with Ficus species in the section Malvanthera. We compare the phylogenies of 15 matched Pleistodontes/Sycoscapter species pairs and show that the level of cospeciation is significantly greater than that expected by chance. Our estimates of the maximum level of cospeciation (50 to 64% of nodes) are very similar to those obtained in other recent studies of coevolved parasitic and mutualistic associations. However, we also show that there is not perfect congruence of pollinator and parasite phylogenies (for any substantial clade) and argue that host plant switching is likely to be less constrained for Sycoscapter parasites than for Pleistodontes pollinators. There is perfect correspondence between two terminal clades of two sister species in the respective phylogenies, and rates of molecular evolution in these pairs are similar.     

Exceptions to the one:one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios

Abstract. The mutualistic breeding system involving fig trees (Moraceae, Ficus ) and fig wasps (Hymenoptera, Chalcidoidea, Agaoninae) would appear so specialized that one may wonder at the evolutionary processes that could be responsible for the existence of about 750 species-specific associations. In this paper we present data concerning two cases of species specificity breakdown between African fig trees and fig wasps. We then analyse the possible evolutionary scenarios which could be responsible, as well as the possible evolutionary outcomes of the observed situations. Our analyses range in scale from continental to habitats, and fig crops to individual figs (syconia). Habitat shifts and ecological barriers seem to be the more likely explanations for the evolution of novel fig tree-fig wasp associations, but sympatric and parapatric scenarios cannot be ruled out.     

比较钝叶榕的三种传粉者及其传粉效率

钝叶榕 (Ficus curtipes)是雌雄同株,它除了依赖钝叶榕传粉榕小蜂Eupristina sp.传粉外,另外两种进入果内繁殖的杨氏榕树金小蜂Diaziella yangi 和Lipothymus sp.金小蜂也能有效地为它传粉,这3种小蜂同时产卵于雌花的子房内,在榕果内繁殖后代.通过控制性放蜂试验,比较研究钝叶榕3种传粉者的传粉效率,结果表明:自然状态下,3种小蜂在绝大多数榕果里只各进1头.在控制性放蜂试验中,3种小蜂的传粉效率均随着放入雌蜂数量的增加而增加,两种金小蜂的传粉效率有时比钝叶榕传粉榕小蜂的传粉效率还高.当钝叶榕传粉榕小蜂分别与两种金小蜂同时放入榕果内传粉时,其生产的种子数量居于或者是接近两种小蜂单独传粉时形成的种子数量,传粉效率没有显著增加.在比较3种小蜂单种分别放1头和2头的传粉效率时,增加单果放蜂数量,钝叶榕传粉榕小蜂和Lipothymus sp. 的平均传粉效率降低,但杨氏榕树金小蜂的平均传粉效率是增加的.对3种不同属传粉小蜂传粉效率的比较,可为研究榕-蜂互惠系统的互惠的起源提供依据.     

Disturbance effects on community structure of Ficus tinctoria fig wasps in Xishuangbanna, China: Implications for the fig/fig wasp mutualism

Abstract  Fig trees are important components of tropical forests, because their fruits are eaten by so many vertebrates, but they depend on pollinating fig wasps to produce mature fruits. Disturbance to habitat structure can have a major impact on insect diversity and composition, potentially reducing fruit yields. We investigated the impact of habitat disturbance on the fig wasp community associated with male figs of Ficus tinctoria in Xishuangbanna, China. The community comprised one pollinator species Liporrhopalum gibbosae and six non-pollinating wasp species: Sycoscapter sp.1, Philotrypesis ravii , Philotrypesis sp.1, Neosycophila omeomorpha , Sycophila sp.1, and Walkerella sp.1. More disturbed areas were characterized by higher temperatures, less shade, and more vehicle noise. The response of the fig wasp community was complex, with no simple relationship between intensity of disturbance and pollinator abundance. However, the sex ratios (proportion of male progeny) of pollinators increased significantly in more disturbed areas. We conclude that potential changes in fig wasp community composition brought about by disturbance, are unpredictable, with unclear consequences for tropical rainforest biodiversity.     

Permeability of receptive fig fruits and its effects on the re‐emergence behaviour of pollinators

1. Figs and pollinating fig wasps provide a model system for studying mutualism. The permeability of the syconium changes during receptivity or between seasons, which may affect the behaviour of pollinators. Fig fruits are permeable during receptivity, and in some species, pollinators can enter and re‐emerge after oviposition/pollination. We studied the relationship between fig permeability and pollinator re‐emergence behaviour with a functional dioecious fig, Ficus hispida and the obligate pollinator Ceratosolen solmsi marchali. 2. The relationship reflects the interaction of figs and pollinators in the mutualism and also the conflicts of interests between the two partners: figs benefit from the enclosed fig fruits which have low permeability, but pollinators benefit from their re‐emergence behaviour, which requires high fig permeability. 3. The results showed that at the end of receptivity, the permeability of fig fruits lowered rapidly with changes to the ostiole structures, and re‐emergence rate was low, with more re‐emerging pollinators trapped in the ostiolar bracts. Our results also showed that in the rainy season, the length of receptivity was shorter and fig permeability was lower. The re‐emergence rates were also lower than those in the dry season. The results elucidated that figs' interests dominated in the conflicts between fig and pollinating wasp. 4. Based on a new criteria which employed the classification of pollinators found dead in the ostiolar bracts and which involved a survey of 6 monoecious and 12 dioecious fig species, we found that re‐emergence behaviour was prevalent among fig species, and was more prevalent in functional dioecious figs than monoecious ones.     

How to be a fig wasp down under: The diversity and structure of an Australian fig wasp community

Endophytic insects and their parasitoids provide valuable models for community ecology. The wasp communities in inflorescences of fig trees have great potential for comparative studies, but we must first describe individual communities. Here, we add to the few detailed studies of such communities by describing the one associated with Ficus rubiginosa in Australia. First, we describe community composition, using two different sampling procedures. Overall, we identified 14 species of non-pollinating fig wasp (NPFW) that fall into two size classes. Small wasps, including pollinators, gallers and their parasitoids, were more abundant than large wasps (both galler and parasitoid species). We show that in figs where wasps emerge naturally, the presence of large wasps may partly explain the low emergence of small wasps. During fig development, large gallers oviposit first, before and around the time of pollination, while parasitoids lay eggs after pollination. We further show that parasitoids in the subfamily Sycoryctinae, which comprise the majority of all individual NPFWs, segregate temporally by laying eggs at different stages of fig development. We discuss our results in terms of species co-existence and community structure and compare our findings to those from fig wasp communities on other continents.     

Non-additive effects of herbivores and pollinators on Erysimum mediohispanicum (Cruciferae) fitness

In this study, the non-additivity of effects of herbivores and pollinator on fitness of the plant Erysimum mediohispanicum (Cruciferae) has been experimentally tested. The abundance and diversity of the pollinator assemblage of plants excluded from and exposed to mammalian herbivores, and the combined effect of pollinators and herbivores on plant reproduction were determined over a period of 2 years. Pollinator abundance was higher and diversity was lower on plants excluded from herbivores. Furthermore, the experimental exclusions demonstrated that both pollinators and herbivores affected plant fitness, but their effects were not independent. Herbivores only had a detrimental effect on plant fitness when pollinators were present. Similarly, pollinators enhanced fitness only when herbivores were excluded. This outcome demonstrates that the importance of pollinators for plant fitness depends on the occurrence of herbivores, and suggests that herbivores may hamper pollinator-mediated adaptation in plants.     

Parasitism of a pollinator fig wasp: mortalities are higher in figs with more pollinators,but are not related to local densities of figs

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Making the most of your pollinators: An epiphytic fig tree encourages its pollinators to roam between figs

Ficus species are characterized by their unusual enclosed inflorescences (figs) and their relationship with obligate pollinator fig wasps (Agaonidae). Fig trees have a variety of growth forms, but true epiphytes are rare, and one example is Ficus deltoidea of Southeast Asia. Presumably as an adaptation to epiphytism, inflorescence design in this species is exceptional, with very few flowers in female (seed‐producing) figs and unusually large seeds. Figs on male (pollinator offspring‐generating) trees have many more flowers. Many fig wasps pollinate one fig each, but because of the low number of flowers per fig, efficient utilization by F. deltoidea''s pollinators depends on pollinators entering several female figs. We hypothesized that it is in the interest of the plants to allow pollinators to re‐emerge from figs on both male and female trees and that selection favors pollinator roaming because it increases their own reproductive success. Our manipulations of Blastophaga sp. pollinators in a Malaysian oil palm plantation confirmed that individual pollinators do routinely enter several figs of both sexes. Entering additional figs generated more seeds per pollinator on female trees and more pollinator offspring on male trees. Offspring sex ratios in subsequently entered figs were often less female‐biased than in the first figs they entered, which reduced their immediate value to male trees because only female offspring carry their pollen. Small numbers of large seeds in female figs of epiphytic F. deltoidea may reflect constraints on overall female fig size, because pollinator exploitation depends on mutual mimicry between male and female figs.     

Improving species distribution models using biotic interactions: a case study of parasites,pollinators and plants

Biotic interactions have been considered as an important factor to be included in species distribution modelling, but little is known about how different types of interaction or different strategies for modelling affect model performance. This study compares different methods for including interspecific interactions in distribution models for bees, their brood parasites, and the plants they pollinate. Host–parasite interactions among bumble bees (genus Bombus: generalist pollinators and brood parasites) and specialist plant–pollinator interactions between Centris bees and Krameria flowers were used as case studies. We used 7 different modelling algorithms available in the BIOMOD R package. For Bombus, the inclusion of interacting species distributions generally increased model predictive accuracy. The improvement was better when the interacting species was included with its raw distribution rather than with its modeled suitability. However, incorporating the distributions of non‐interacting species sometimes resulted in similarly increased model accuracy despite their being no significance of any interaction for the distribution. For the Centris‐Krameria system the best strategy for modelling biotic interactions was to include the interacting species model‐predicted values. However, the results were less consistent than those for Bombus species, and most models including biotic interactions showed no significant improvement over abiotic models. Our results are consistent with previous studies showing that biotic interactions can be important in structuring species distributions at regional scales. However, correlations between species distributions are not necessarily indicative of interactions. Therefore, choosing the correct biotic information, based on biological and ecological knowledge, is critical to improve the accuracy of species distribution models and forecast distribution change.     

Persistence of a fig wasp population and evolution of dioecy in figs: a simulation study

The relationship between fig trees and their pollinator wasps is a well-known example of species-specific obligate mutualism. In this article we present a stochastic model of this mutualistic system, referring to data on a dioecious fig (Ficus schwarzii) in Borneo, and examine the conditions for the persistence of a wasp population for a given period. (1) When the average duration of the flowering interval of fig trees is short, even a small fig population can sustain a wasp population successfully. A population whose average period of flowering cycle is half that of another population can sustain a wasp population with a number of trees less than half of the other population. (2) The wasp survival rate (WSR) is higher when (a) the variation of the interval periods of fig flowering is smaller, (b) the fig population size is larger, and (c) figs can prolong their receptivity to wait for a wasp if no wasps are available. (3) WSR is predictable from the average proportion of the fig's receptive phases, in which wasps are available, to their total receptive phases. (4) The persistence period of a wasp population increases exponentially with the number of fig trees. Based on these results we propose a new hypothesis, as a possible scenario, on the evolution of dioecy from monoecy in Ficus. Received: November 13, 1998 / Accepted: July 14, 1999     

The effects of urbanization on pollinators and pollination: A meta-analysis

Urbanization is increasing worldwide, with major impacts on biodiversity, species interactions and ecosystem functioning. Pollination is an ecosystem function vital for terrestrial ecosystems and food security; however, the processes underlying the patterns of pollinator diversity and the ecosystem services they provide in cities have seldom been quantified. Here, we perform a comprehensive meta-analysis of 133 studies examining the effects of urbanization on pollinators and pollination. Our results confirm the widespread negative impacts of urbanization on pollinator richness and abundance, with Lepidoptera being the most affected group. Furthermore, pollinator responses were found to be trait-specific, with below-ground nesting and solitary Hymenoptera, and spring flyers more severely affected by urbanization. Meanwhile, cities promote non-native pollinators, which may exacerbate conservation risks to native species. Surprisingly, despite the negative effects of urbanization on pollinator diversity, pollination service measured as seed set is enhanced in non-tropical cities likely due to abundant generalists and managed pollinators therein. We emphasize that the richness of local flowering plants could mitigate the negative impacts of urbanization on pollinator diversity. Overall, the results demonstrate the varying magnitudes of multiple moderators on urban pollinators and pollination services and could help guide conservation actions for biodiversity and ecosystem function for a sustainable future.     

Detecting the elusive cost of parasites on fig seed production

Mutualisms provide essential ecosystem functions such as pollination and contribute considerably to global biodiversity. However, they are also exploited by parasites that remove resources and thus impose costs on one or both of the mutualistic partners. The fig/pollinator interaction is a classic obligate mutualism; it is pantropical and involves >750 Ficus species and their host-specific pollinating wasps (family Agaonidae). Figs also host parasites of the mutualism that should consume pollinators or seeds, depending on their larval ecology. We collected data from a large crop of figs on Ficus glandifera var. brachysyce in a Sulawesi rainforest with an unusually high number of Eukoebelea sp. parasites. We found that these parasites have a significant negative correlation with fig seed production as well as with pollinator offspring production. Eukoebelea wasps form the basal genus in subfamily Sycophaginae (Chalcidoidea) and their larval biology is considered unknown. Our analysis suggests that they feed as flower gallers and impose direct costs on the fig tree, but a strategy including the consumption of pollinator larvae cannot be ruled out. We also present baseline data on the composition of the fig wasp community associated with F. glandifera var brachysyce and light trap catch data.     

Precision of host sanctions in the fig tree–fig wasp mutualism: consequences for uncooperative symbionts

Host sanctions that reduce the relative fitness of uncooperative symbionts provide a mechanism that can limit cheating and thus stabilise mutualisms over evolutionary timescales. Sanctions have been demonstrated empirically in several mutualisms. However, if multiple individual symbionts interact with each host, the precision with which individual cheating symbionts are targeted by host sanctions is critical to their short‐ and long‐term effectiveness. No previous empirical study has directly addressed this issue. Here, we report the precision of host sanctions in the mutualism between fig trees and their pollinating wasps. Using field experiments and molecular parentage analyses, we show that sanctions in Ficus nymphaeifolia act at the level of entire figs (syconia), not at the level of the individual flowers within. Such fig‐level sanctions allow uncooperative wasps, which do not bring pollen, to avoid sanctions in figs to which other wasps bring pollen. We discuss the relevance of sanction precision to other mutualisms.     

Inbreeding effects on fitness traits in the heterocarpic herb Leontodon autumnalis L. (Asteraceae)

Heterocarpic plants are characterized by the production of distinct types of fruits that usually differ in their ecological behavior. In the Asteraceae, differences are mainly found between peripheral non-dispersal and central dispersal achenes (single-seeded fruits). Inbreeding depression is considered as an evolutionary force as it may reduce several fitness traits, and in the case of heterocarpic plants, it could influence fitness traits (e.g., seed set, germination rate, growth rate) of each fruit morph, which may have important ecological and evolutionary consequences. In particular, differential effects on fitness traits and dispersal of selfed and outcrossed progeny can strongly determine the viability of extant populations and the potential to colonize new habitats. We conducted a hand-pollination experiment in greenhouse conditions to test whether inbreeding affects the fitness of achene morphs in the heterocarpic herb Leontodon autumnalis (Asteraceae). Results show that achene morphs significantly differ in their ecological behavior, peripheral achenes germinating more and faster than central achenes. The significant interaction between pollination treatment and achene morph for germination probability might indicate a link between dormancy and mating system in L. autumnalis: germination was higher for outcrossed achenes in central achenes whereas the opposite pattern was exhibited by peripheral achenes. Selfing dramatically reduced seed set, probably as a consequence of strong self-incompatibility mechanisms rather than inbreeding effects. Inbreeding depression significantly affected late life-cycle traits, such as growth rate and biomass at flowering. Overall, results suggest that inbreeding depression seems to be an important selective force maintaining outcrossing in L. autumnalis.     

Interactions between isolates of the entomopathogenic fungus Metarhizium anisopliae and the entomopathogenic nematode Heterorhabditis bacteriophora JPM4 during infection of the sugar cane borer Diatraea saccharalis (Lepidoptera: Pyralidae)

Interactions between the nematode Heterorhabditis bacteriophora isolate JPM4 and the fungus Metarhizium anisopliae, isolates LPP45 and LPP39, were studied during dual infections of Diatraea saccharalis. Mortality, production of infective juveniles (IJs) and production of conidia were evaluated. A positive effect was demonstrated for host mortality in duel infections of JPM4 and LPP39, causing 100% mortality with LT₅₀ and LT₉₅ values of 1.8 and 2.8 days, respectively. Higher values were seen when using the nematode or fungi individually. However, a combination of JPM4 + LPP39 caused a significant reduction in IJ production. The results show that faster time to death, a moderately virulent fungal isolate could be combined with the nematode, however at the expense of IJ production.     

High incidences and similar patterns of Wolbachia infection in fig wasp communities from three different continents

Abstract Wolbachia are endosymbiotic bacteria that infect numerous arthropod species. Previous studies in Panama and Australia revealed that the majority of fig wasp species harbor Wolbachia infections, but that similar patterns of incidence have evolved independently with different wasp species and Wolbachia strains on the two continents. We found Wolbachia infections in 25/47 species (53%) of fig wasp associated with 25 species of Chinese figs. Phylogenetic analyses of Wolbachia wsp sequences indicated that very similar strains are not obviously found in either closely related or ecologically linked fig wasps species. The extremely high prevalence of Wolbachia in fig wasps (over 50% of species infected) is not constrained by geographical origin and is a recurrent theme of fig wasp/Wolbachia interactions.     

Isolation of six microsatellite loci in the pollinating fig wasp,Platyscapa awekei

Platyscapa awekei DNA was enriched for several repeat motifs. Sequencing of 48 transformed colonies showed that 22 contained microsatellite loci. Eleven of these loci were tested and six of them proved to be reliable and variable. As expected from these wasps’ biology, F_IS was high (= 0.423), indicating frequent sibmating. Notwithstanding, we estimate that dispersing males may secure as much as 8% of all matings.     

Testing the emergence of New Caledonia: fig wasp mutualism as a case study and a review of evidence

While geologists suggest that New Caledonian main island (Grande Terre) was submerged until ca 37 Ma, biologists are struck by the presence of supposedly Gondwanan groups on the island. Among these groups are the Oreosycea fig trees (Ficus, Moraceae) and their Dolichoris pollinators (Hymenoptera, Agaonidae). These partners are distributed in the Paleotropics and Australasia, suggesting that their presence on New Caledonia could result from Gondwanan vicariance. To test this hypothesis, we obtained mitochondrial and nuclear markers (5.3 kb) from 28 species of Dolichoris, used all available sequences for Oreosycea, and conducted phylogenetic and dating analyses with several calibration strategies. All our analyses ruled out a vicariance scenario suggesting instead that New Caledonian colonization by Dolichoris and Oreosycea involved dispersal across islands from Sundaland ca 45.9-32.0 Ma. Our results show that successful long-distance dispersal of obligate mutualists may happen further suggesting that presence of intimate mutualisms on isolated islands should not be used as a priori evidence for vicariance. Comparing our results to a review of all the published age estimates for New Caledonian plant and animal taxa, we showed that support for a vicariant origin of the island biota is still lacking. Finally, as demonstrating a causal relationship between geology and biology requires independent evidence, we argue that a priori assumptions about vicariance or dispersal should not be used to constrain chronograms. This circular reasoning could lead to under or overestimation of age estimates.