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Spatial Stratification of Internally and Externally Non-Pollinating Fig Wasps and Their Effects on Pollinator and Seed Abundance in Ficus burkei  [PDF]
Sarah Al-Beidh,Derek W. Dunn,James M. Cook
ISRN Zoology , 2012, DOI: 10.5402/2012/908560
Abstract: Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms. 1. Introduction Mutualisms are reciprocally beneficial interspecific interactions [1, 2], and a well-known system is that between fig trees (Ficus spp.) and their agaonid wasp pollinators [3–6]. In return for pollination, the wasps gall some fig ovules, which are then eaten by the larvae. About half (300+) of Ficus species are monoecious, where both male flowers and ovules are present in the same syconium (enclosed inflorescence or “fig”). Within monoecious syconia, ovules are highly variable in length [7–10]. Long (inner) ovules have short styles and mature near the centre of the syconium, whereas short (outer), long-styled ovules mature nearer the outer wall (see Figure 1). Female pollinating wasps (foundresses) lay their eggs by inserting their ovipositors down the flower styles. At maturation, wasp galls are clustered at the syconium’s centre [4, 6, 9–13] with seeds at the outer wall. This spatial stratification of pollinating wasps and seeds enables mutualism stability, although the mechanisms preventing the wasps from galling all ovules are unclear. Figure 1: Variation in style and pedicel length in female flowers of monoecious Ficus (adapted from Dunn et al. [ 13]). Mechanisms proposed to
Diet of Non-pollinating Wasps and Their Impact on the Stability of Fig-pollinator Wasp Mutualism

YANG Cheng-yun,WANG Rui-Wu,ZHAO Gui-Fang,YANG Da-Rong,

动物学研究 , 2005,
Abstract: Ficus (Moraceae) and their species-specific pollinator wasps (Agaonidae) form a remarkable plant-insect obligate mutualism, and non-pollinators are the exploiters of the mutualism. The negative impact of exploiters on the reciprocal mutualists might disrupt the reciprocal mutualism in the process of evolution, but how the exploiters could coexist with the reciprocal mutualsits is not still clear. In this study, the diet of the five species of non-pollinators and relationship among fig wasps were analyzed on Ficus racemosa L. in Xishuangbanna from Dec. 2003 to Apr. 2004. In a controlled experiment pollinators and each species of non-pollinators oviposited and counts of wasps and seeds in mature figs were conducted. The results indicated that only Platyneura testacea Motschulsky and Platyneura mayri Rasplus are gall-makers, which can induce the ovaries into galls; Apocrypta sp., Apocrypta westwoodi Grandi and Platyneura agraensis Joseph are the parasitoids. The gall-makers and the parasitoids of pollinators have negative impacts on pollinators, but the impacts are not significant because of the influence of the ants and parasitoids of gall-makers. Additionally, the experiment excluding non-pollinators oviposition showed that the number of offspring of pollinators and seeds were not significantly different with the natural fruits. Moreover, the analysis on the natural population structure of fig wasps revealed that the pollinators are the dominant species. So in the natural condition, the abundance of gall-makers and parasitoids of pollinators are below the level needed to exclude pollinators, and thus they have a relatively weak impact on the stability of fig-pollinator mutualism and can coexist with the mutualism.
Evolution and Expression Plasticity of Opsin Genes in a Fig Pollinator, Ceratosolen solmsi  [PDF]
Bo Wang, Jin-Hua Xiao, Sheng-Nan Bian, Li-Ming Niu, Robert W. Murphy, Da-Wei Huang
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0053907
Abstract: Figs and fig pollinators have co-evolved species-specific systems of mutualism. So far, it was unknown how visual opsin genes of pollinators have evolved in the light conditions inside their host figs. We cloned intact full-length mRNA sequences of four opsin genes from a species of fig pollinator, Ceratosolen solmsi, and tested for selective pressure and expressional plasticity of these genes. Molecular evolutionary analysis indicated that the four opsin genes evolved under different selective constraints. Subsets of codons in the two long wavelength sensitive opsin (LW1, LW2) genes were positively selected in ancestral fig pollinators. The ultraviolet sensitive opsin (UV) gene was under strong purifying selection, whereas a relaxation of selective constrains occurred on several amino acids in the blue opsin. RT-qPCR analysis suggested that female and male fig pollinators had different expression patterns possibly due to their distinct lifestyles and different responses to light within the syconia. Co-evolutionary history with figs might have influenced the evolution and expression plasticity of opsin genes in fig pollinators.

植物生态学报 , 2004,
Abstract: Ficus is the keystone plant in tropical forests, and it also occurs in subtropical and even temperate areas. More than 700 species in the genus Ficus (Moraceae: Ficus ) and their species_specific pollinator, the fig wasp, (Chalcidoidae: Agaonidae) has been discovered. The interactions between them, which have become an obligate mutualist relationship, have a very long evolutionary history. Pollen dispersal in figs is completely dependent on fig wasps, which enter the syconium where viable seeds are produced. Fig pollinators are uniquely dependent on the fig for the completion of their life cycle. Each fig species attracts its own species of fig wasp by emitting specific volatile compounds during their receptive period and these wasps lay their eggs in the developing ovary of the host fig species. As ovipositing female wasps simultaneously carry pollen from other syconia and pollinate figs actively or passively, they show peculiar morphological and behavioral adaptations to figs and a life cycle highly synchronous with fig inflorescence. Such specialization and interactions make diversity in species, genetics, morphology and behavior in pollinators and their host plants an exciting example for studying interspecific coevolution. Although fig_pollinator symbiosis is now widely regarded as a model system of plant_insect coevolved mutualism, little is known about the history and process of their interactions. Current experiments and observations have suggested the fig/fig wasp obligate mutualism (this is not a complete sentence but I am not sure what the author is trying to say here). However, present fig and fig wasp classifications, which are based on morphological characteristics and their interactions, are still incomplete and controversial. This short review summarized the knowledge and questions on coevolved mutualism, the molecular phylogeny of fig/fig pollinator symbionts and the traditional classification of Ficus . Studies on the interactions between fig/fig pollinator and re_classification of Ficus in China based on molecular phylogeny were also discussed. Research on the phylogeny of about 100 species of fig trees, which mainly occur in tropical and subtropical areas in China, has just started and only a few reports on fig pollination biology and ecology exist. Much work should be done to make a thorough study of both symbiotic partners. Though systematic classification of Ficus is the basis of the coevolutionary study, application of molecular phylogeny is also necessary and feasible, which will promote further research and understanding of plant_insect coevolution in China.
Interference Competition and High Temperatures Reduce the Virulence of Fig Wasps and Stabilize a Fig-Wasp Mutualism  [PDF]
Rui-Wu Wang,Jo Ridley,Bao-Fa Sun,Qi Zheng,Derek W. Dunn,James Cook,Lei Shi,Ya-Ping Zhang,Douglas W. Yu
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0007802
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.
A study on pollination ecology of Ficus virens and its insect pollinators

CHEN Yong,

生态学报 , 2001,
Abstract: Ficus virens is monoecious,with each syconium bearing both male and female flowers.The female flowers are divided into long-styled flowers and short-styled ones,but both bear fruits and form galls and are not separated physicologically.In these syconia live 4 kinds of insects of Chalcidoidea,of which two species of Agaonidae are the pollinators of Ficus virens,especially Blastophaga sp.is a main pollinator of Ficus virens and a legitimate companion of the mutualism system.Blastophaga coronata is the secondary pollinator and also the competitor of the main pollinator.Sycophila and Ormyrus are the parasites of the above two fig wasps,but male Ormyrus sp.also takes part in digging holes of dispersal in the syconia.This article for the first time reports the mutualism relationship between fig trees with monoecism and its pollinators under the seasonal environmental stress in China.The article also discusses the sustaining countermeasures of the mutualism system.
Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism
Michael J McLeish, Simon van Noort
BMC Evolutionary Biology , 2012, DOI: 10.1186/1471-2148-12-1
Abstract: Statistical parsimony and AMOVA revealed deep divergences at the COI locus within several pollinating fig wasp species that persist on the same host Ficus species. Changes in branching patterns estimated using the generalized mixed Yule coalescent test indicated lineage duplication on the same Ficus species. Conversely, Elisabethiella and Alfonsiella fig wasp species are able to reproduce on multiple, but closely related host fig species. Tree reconciliation tests indicate significant codiversification as well as significant incongruence between fig wasp and Ficus phylogenies.The findings demonstrate more relaxed pollinating fig wasp host specificity than previously appreciated. Evolutionarily conservative host associations have been tempered by horizontal transfer and lineage duplication among closely related Ficus species. Independent and asynchronistic diversification of pollinating fig wasps is best explained by a combination of both sympatric and allopatric models of speciation. Pollinator host preference constraints permit reproduction on closely related Ficus species, but uncertainty of the frequency and duration of these associations requires better resolution.Several lines of theory have been proposed to account for the enormous diversity of phytophagous insects. Diversification conceivably ensues by ecological opportunity and adaptation to the exploitation of previously unattainable resources [1,2]; by restricted gene flow through allopatric means [3,4]; and disruptive selection and sympatric speciation [5,6]. In order to discern among potential mechanisms driving speciation, both historical pattern and ecological scale processes are important to consider [7-10]. Comparative phylogenetic approaches that test congruence between host and associate populations can contribute to greater resolution in unravelling ecological scale processes [11-14]. Here we interpret the codiversification between Ficus host species and populations of a group of African fig wasp
Reproductive Characters of Ficus hirta Vahl (Moraceae) and its Symbiotic Fig Wasps
粗叶榕(Ficus hirta)繁殖系统的特征及其共生的榕小蜂

植物学报 , 2004,
Abstract: Morphology and syconium structure of Ficus hirta Vahl, the reproductive traints of host and its symbiotic wasps, and some basic features of their mutualism system, are discussed. In gall figs, there are 3 species of fig wasps (Chalcidoidea: Hymenoptera), one of which is a legitimate pollinator, Blastophaga javana of Agaoninae, the other two are nonpollinators, Sycoscapter sp. and Philotrypesis sp. (Sycoryctinae) which oviposit outside syconium.
Plant chemical defence: a partner control mechanism stabilising plant - seed-eating pollinator mutualisms
Sébastien Ibanez, Christiane Gallet, Fanny Dommanget, Laurence Després
BMC Evolutionary Biology , 2009, DOI: 10.1186/1471-2148-9-261
Abstract: This study shows that plant chemical defence against developing larvae constitutes another partner sanction mechanism in nursery mutualisms. It documents the chemical defence used by globeflower Trollius europaeus L. (Ranunculaceae) against the seed-eating larvae of six pollinating species of the genus Chiastocheta Pokorny (Anthomyiidae). The correlative field study carried out shows that the severity of damage caused by Chiastocheta larvae to globeflower fruits is linked to the accumulation in the carpel walls of a C-glycosyl-flavone (adonivernith), which reduces the larval seed predation ability per damaged carpel. The different Chiastocheta species do not exploit the fruit in the same way and their interaction with the plant chemical defence is variable, both in terms of induction intensity and larval sensitivity to adonivernith.Adonivernith accumulation and larval predation intensity appear to be both the reciprocal cause and effect. Adonivernith not only constitutes an effective chemical means of partner control, but may also play a key role in the sympatric diversification of the Chiastocheta genus.Conflicts of interest are frequent in interspecific mutualisms [1,2]. Plant/seed-eating pollinator mutualisms involve a plant pollinated by an insect whose larvae develop upon the plant's seeds. In these nursery pollination mutualisms, the conflict lies in the number of seeds eaten by the pollinator's larvae that therefore will not contribute to the plant's fitness [3-6]. As a consequence, evolutionary theory predicts that plants evolve traits that limit the costs imposed by the insect partners. Despite this broad prediction, attempts to identify mechanisms of partner control in nursery mutualisms have so far fell short in pinpointing a general mechanism. Pellmyr & Huth [7] showed that the selective abortion of fruits in the Yucca - Yucca moth interaction was an effective defence against the developing larvae, but this mechanism was found in only one of the three Yu
The mating behaviors of the non-pollinating fig wasps of Ficus curtipes
钝叶榕(Ficus curtipes)非传粉小蜂交配行为

SONG Bo,PENG Yan-Qiong,YANG Zhao-Xiong,YANG Da-Rong,

生态学报 , 2008,
Abstract: Ficus and their species-specific pollinator wasps (Agaonidae) exhibit a remarkable obligate mutualism. Fig trees are typically pollinated only by female agaonids, whose offspring feed on the ovules of the plant. Figs also shelter numerous other, unrelated, fig wasps that usually exploit the fig pollinator mutualism. Ficus curtipes Corner is a monoecious strangler fig tree. At Xishuangbanna Tropical Botanical Garden, 9493 individual fig wasps were reared from 100 figs (syconia). They included one species of agaonid wasp and five unrelated fig wasps. The agaonid Eupristina sp. was represented by 45% of the individuals, Diaziella yangi van Noort & Rasplus by 46% and the remaining 9% by Lipothymus sp., Philotrypesis sp., Sycobia sp. and Sycoscopter sp. Females of the first three species enter the figs to oviposit whereas the others lay their eggs from the outside of the figs. In this study, the order of emergence of the fig wasps from their natal figs and their mating behavior were recorded. They followed a strict sequence of emergence, with Sycobia sp. emerging first, then Lipothymus sp., followed by Diaziella yangi. Eupristina sp., Philotrypesis sp. and Sycoscopter sp. emerged last. Contrary to expectations, the mating sites of the five species of non-agaonid fig wasps were not always linked to the presence or absence of wings in the males. D. yangi (with winged males) mated mostly inside the figs and its males engaged in fatal fights for mating opportunities. Male Lipothymus sp. (with wingless males), mated both inside and outside the figs whereas male Sycobia sp. (with winged males) only mated outside. Males of Philotrypesis sp. and Sycoscopter sp. (both with wingless males), only mated inside the figs. Fig wasps often display highly female-biased sex ratios linked to local mate competition. D. yangi, despite having winged males, mated mainly inside the figs, which is likely to influence its optimal sex ratio. The presence of wings in male fig wasps is therefore not a good predictor of mating sites, nor sex ratio.
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