Pollinator sharing in dioecious figs (Ficus: Moraceae)

As one of the most specialized pollination syndromes, the fig (Ficus)–fig wasp (Agaonidae) mutualism can shed light on how pollinator behaviour and specificity affect plant diversification through processes such as reproductive isolation and hybridization. Pollinator sharing among species has important implications for Ficus species delimitation and the evolutionary history of the mutualism. Although agaonid wasp pollinators are known to visit more than one host species in monoecious figs, pollinator sharing has yet to be documented in dioecious figs. The present study investigated the frequency of pollinator sharing among sympatric, closely‐related dioecious figs in Ficus sections Sycocarpus and Sycidium. Molecular and morphological species identification established the associations between pollinating agaonid wasp species and host fig species. Cytochrome oxidase I was sequenced from 372 Ceratosolen pollinators of Ficus section Sycocarpus and 210 Kradibia pollinators of Ficus section Sycidium. The association between fig species and morphologically distinct clades of pollinator haplotypes was predominantly one‐to‐one. In Ceratosolen, six of 372 pollinators (1.5%) visited fig species other than the predominant host. No pollinator sharing was detected between the two Sycidium host species, although a rare hybrid shared Kradibia pollinators with both parental species. These findings point to low rates of pollinator sharing among closely‐related dioecious fig species in sympatry, and perhaps lower rates than among monoecious figs. Such rare events could be evolutionarily important as mechanisms for gene flow among fig species. Differences in rates of pollinator sharing among fig lineages might explain the conflicting phylogenetic patterns inferred among monoecious figs, dioecious figs, and their respective pollinators. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 546–558.     

The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues

Background and Aims

Pollinator specificity facilitates reproductive isolation among plants, and mechanisms that generate specificity influence species boundaries. Long-range volatile attractants, in combination with morphological co-adaptations, are generally regarded as being responsible for maintaining extreme host specificity among the fig wasps that pollinate fig trees, but increasing evidence for breakdowns in specificity is accumulating. The basis of host specificity was examined among two host-specific Ceratosolen fig wasps that pollinate two sympatric varieties of Ficus semicordata, together with the consequences for the plants when pollinators entered the alternative host variety.

Methods

The compositions of floral scents from receptive figs of the two varieties and responses of their pollinators to these volatiles were compared. The behaviour of the wasps once on the surface of the figs was also recorded, together with the reproductive success of figs entered by the two Ceratosolen species.

Key Results

The receptive-phase floral scents of the two varieties had different chemical compositions, but only one Ceratosolen species displayed a preference between them in Y-tube trials. Specificity was reinforced at a later stage, once pollinators were walking on the figs, because both species preferred to enter figs of their normal hosts. Both pollinators could enter figs of both varieties and pollinate them, but figs with extra-varietal pollen were more likely to abort and contained fewer seeds. Hybrid seeds germinated at normal rates.

Conclusions

Contact cues on the surface of figs have been largely ignored in previous studies of fig wasp host preferences, but together with floral scents they maintain host specificity among the pollinators of sympatric F. semicordata varieties. When pollinators enter atypical hosts, post-zygotic factors reduce but do not prevent the production of hybrid offspring, suggesting there may be gene flow between these varieties.     

Insect responses to host plant provision beyond natural boundaries: latitudinal and altitudinal variation in a Chinese fig wasp community

Many plants are grown outside their natural ranges. Plantings adjacent to native ranges provide an opportunity to monitor community assembly among associated insects and their parasitoids in novel environments, to determine whether gradients in species richness emerge and to examine their consequences for host plant reproductive success. We recorded the fig wasps (Chalcidoidea) associated with a single plant resource (ovules of Ficus microcarpa) along a 1200 km transect in southwest China that extended for 1000 km beyond the tree's natural northern range margin. The fig wasps included the tree's agaonid pollinator and other species that feed on the ovules or are their parasitoids. Phytophagous fig wasps (12 species) were more numerous than parasitoids (nine species). The proportion of figs occupied by fig wasps declined with increasing latitude, as did the proportion of utilized ovules in occupied figs. Species richness, diversity, and abundance of fig wasps also significantly changed along both latitudinal and altitudinal gradients. Parasitoids declined more steeply with latitude than phytophages. Seed production declined beyond the natural northern range margin, and at high elevation, because pollinator fig wasps became rare or absent. This suggests that pollinator climatic tolerances helped limit the tree's natural distribution, although competition with another species may have excluded pollinators at the highest altitude site. Isolation by distance may prevent colonization of northern sites by some fig wasps and act in combination with direct and host‐mediated climatic effects to generate gradients in community composition, with parasitoids inherently more sensitive because of declines in the abundance of potential hosts.     

Pollinators entering female dioecious figs: why commit suicide?

In the dioecious fig/pollinator mutualism, the female wasps that pollinate figs on female trees die without reproducing, whereas wasps that pollinate figs on male trees produce offspring. Selection should strongly favour wasps that avoid female figs and enter only male figs. Consequently, fig trees would not be pollinated and fig seed production would ultimately cease, leading to extinction of both wasp and fig. We experimentally presented pollinators in the wild (southern India) with a choice between male and female figs of a dioecious fig species, Ficus hispida L. Our results show that wasps do not systematically discriminate between sexes of F. hispida. We propose four hypotheses to explain why wasp choice has not evolved, and how a mutualism is thus maintained in which all wasps that pollinate female figs have zero fitness.     

Seasonal change in the structure of fig-wasp community and its implication for conservation

Figs (Moraceae) and their pollinating wasps (Agaonidae) constitute a famous reciprocal mutualism in which figs provide some female flowers for the development of fig wasp offspring while the fig wasps pollinate fig flowers. However, figs also host many non-pollinating wasps which are either parasitoids or resource competitors of pollinators, and bring no benefit for figs and are detrimental to fig’ fitness. Our data onFicus racemosa in Xishuangbanna showed that the numbers of non-pollinators and the mature syconia without pollinator wasps increase in rainy season, especially in the highly fragmented forest. This might be because of the longer developing time of the syconia and thereby longer oviposition time to non-pollinators in the dry season. The galled flower and the viable seed percentages in dry seasons are also larger than in rainy seasons in both primary forest and fragmented forest, and the development of non-pollinators is mainly at the expense of pollinator wasps. Our results showed that there exists a discriminative seasonal impact of non-pollinators and fragmentation effects on population size of fig’s pollinators. This implies that fig/fig wasp mutualism is more fragile in dry season, and that the critical population size and breeding units of figs in seasonal area might be larger than previously estimated without considering the seasonal change of pollinator population.     

Between‐species facilitation by male fig wasps in shared figs

1. Facilitation is recorded from diverse plant–insect interactions, including pollination and herbivory. 2. The significance of facilitation resulting from the behavior of males of multiple fig wasp species inside figs was investigated. Female fig wasps emerge from natal figs via exit holes dug by males, especially male pollinators. When no males are present, the females struggle to escape and may die. 3. Ficus microcarpa L. is a widely‐established invasive fig tree from Southeast Asia. Its pollinator is absent in South Africa, so the tree cannot reproduce, but two Asian non‐pollinating fig wasps (NPFW) Walkerella microcarpae and Odontofroggatia galili occupy its figs. Abundance patterns of the two NPFW and the proportion of male‐free figs in South Africa, Spain (where the pollinator is introduced), and in China, where the native fig wasp community is diverse, were compared to determine the consequences of reduced species richness for insect survival. 4. Female fig wasps in male‐free figs were found to be trapped, and small clutch sizes contributed to the absence of males in both species. The presence of pollinators in Spain allowed most NPFW to develop in figs containing males. Far more male‐free figs were present in South Africa, elevating mortality rates among female NPFW. Facilitation of female release by males of other NPFW species nonetheless benefitted the rarer species. 5. Selection pressures in South Africa currently favour greater aggregation of NPFW offspring and/or less female biased sex ratios.     

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

相似文献   

Complementary fruiting phenologies facilitate sharing of one pollinator fig wasp by two fig trees

Aims Most pollinator fig wasps are host plant specific, with each species only breeding in the figs of one fig tree species, but increasing numbers of species are known to be pollinated by more than one fig wasp, and in rare instances host switching can result in Ficus species sharing pollinators. In this study, we examined factors facilitating observed host switching at Xishuangbanna in Southwestern (SW) China, where Ficus squamosa is at the northern edge of its range and lacks the fig wasps that pollinate it elsewhere, and its figs are colonized by a Ceratosolen pollinator that routinely breeds in figs of F. heterostyla .Methods We recorded the habitat preferences of F. squamosa and F. heterostyla at Xishuangbanna, and compared characteristics such as fig size, location and colour at receptive phase. Furthermore, the vegetative and reproductive phenologies in the populations of F. squamosa and F. heterostyla were recorded weekly at Xishuangbanna Tropical Botanical Garden for 1 year.Important findings Ficus squamosa is a shrub found near fast-flowing rivers, F. heterostyla is a small tree of disturbed forest edges. Although preferring different habitats, they can be found growing close together. Both species have figs located at or near ground level, but they differ in size when pollinated. Fig production in F. squamosa was concentrated in the colder months. F. heterostyla produced more figs in summer but had some throughout the year. The absence of its normal pollinators, in combination with similarly located figs and partially complementary fruiting patterns appear to have facilitated colonization of F. squamosa by the routine pollinator of F. heterostyla. The figs probably also share similar attractant volatiles. This host switching suggests one mechanism whereby fig trees can acquire new pollinators and emphasizes the likely significance of edges of ranges in the genesis of novel fig tree–fig wasp relationships.     

Variation in inflorescence size in a dioecious fig tree and its consequences for the plant and its pollinator fig wasp

The host-specific relationship between fig trees (Ficus) and their pollinator wasps (Agaonidae) is a classic case of obligate mutualism. Pollinators reproduce within highly specialised inflorescences (figs) of fig trees that depend on the pollinator offspring for the dispersal of their pollen. About half of all fig trees are functionally dioecious, with separate male and female plants responsible for separate sexual functions. Pollen and the fig wasps that disperse it are produced within male figs, whereas female figs produce only seeds. Figs vary greatly in size between different species, with female flower numbers varying from tens to many thousands. Within species, the number of female flowers present in each fig is potentially a major determinant of the numbers of pollinator offspring and seeds produced. We recorded variation in female flower numbers within male and female figs of the dioecious Ficus montana growing under controlled conditions, and assessed the sources and consequences of inflorescence size variation for the reproductive success of the plants and their pollinator (Kradibia tentacularis). Female flower numbers varied greatly within and between plants, as did the reproductive success of the plants, and their pollinators. The numbers of pollinator offspring in male figs and seeds in female figs were positively correlated with female flower numbers, but the numbers of male flowers and a parasitoid of the pollinator were not. The significant variation in flower number among figs produced by different individuals growing under uniform conditions indicates that there is a genetic influence on inflorescence size and that this character may be subject to selection.     

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

Effects of conspecific and heterospecific floral density on the pollination of two related rewarding orchids

Variation in within-population floral density can affect interactions between plants and pollinators, resulting in variable pollen export for plants. We investigated the effects of conspecific and heterospecific floral densities on pollination success both of two related, self-compatible, nectar-rewarding orchid species in Ireland, Spiranthes romanzoffiana (rare and listed as endangered) and its congener, S. spiralis (more abundant and not of conservation concern). Floral densities, insect visitation rates, and orchid pollen transport were recorded in multiple quadrats in four populations of both orchid species over their flowering season. We found that conspecific and heterospecific co-flowering plant density affected pollination in both orchid species. For S. romanzoffiana, higher heterospecific density increased pollen removal. For S. spiralis, higher conspecific visitation increased pollen removal and increased heterospecific density decreased pollen deposition. In addition, increased conspecific density increased pollen deposition in both species. This study shows that plants may interact to facilitate or compete for different components of the pollination process, namely; pollinator attraction, pollen removal and deposition. Such interactions have immediate consequences for endangered plant species, as increases in both conspecific and heterospecific coflowering density may ameliorate the negative effects of rarity on pollination, hence overall reproductive success.     

Genome‐wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae,Ficus)

The obligate mutualism of figs and fig‐pollinating wasps has been one of the classic models used for testing theories of co‐evolution and cospeciation due to the high species‐specificity of these relationships. To investigate the species‐specificity between figs and fig pollinators and to further understand the speciation process in obligate mutualisms, we examined the genetic differentiation and phylogenetic relationships of four closely related fig‐pollinating wasp species (Blastophaga nipponica, Blastophaga taiwanensis, Blastophaga tannoensis and Blastophaga yeni) in Japan and Taiwan using genome‐wide sequence data, including mitochondrial DNA sequences. In addition, population structure was analysed for the fig wasps and their host species using microsatellite data. The results suggest that the three Taiwanese fig wasp species are a single panmictic population that pollinates three dioecious fig species, which are sympatrically distributed, have large differences in morphology and ecology and are also genetically differentiated. Our results illustrate the first case of pollinator sharing by host shift in the subgenus Ficus. On the other hand, there are strict genetic codivergences between allopatric populations of the two host–pollinator pairs. The possible processes that produce these pollinator‐sharing events are discussed based on the level and pattern of genetic differentiation in these figs and fig wasps.     

Molecular phylogenies of fig pollinating and non-pollinating wasps and the implications for the origin and evolution of the fig-fig wasp mutualism

Abstract. Figs host three ecologically distinct groups of wasps: pollinators, non-pollinators (parasitic wasps) and parasitoids. Both pollinators and non-pollinators complete their life cycles using fig tissue, while parasitoids appear to attack some groups of non-pollinators. We used nucleotide sequence data to address a series of questions concerning genealogical associations, host specificities and degree of strict-sense co-evolution exhibited by members of these groups. We used the relatively conserved 12S rRNA gene of the mitochondria to estimate high level relationships among pollinator, parasitic and parasitoid taxa by sampling species collected from host figs representing five sections (three subgenera) from Asia, Africa, Europe and Central America. We found that all pollinators formed a clear monophyletic group. However, we could not resolve whether or not all of the non-parasitoid wasps associated with figs (Agaonidae, sensu Bouček) formed a single monophyletic group. Further, we used the more variable COII mitochondrial gene to attempt to determine relationships among closely related species of pollinators within two New World genera. Using sequences from the same gene we estimated the phylogenetic relationships among the parasites collected from the same New World host fig species and compared them with those of the pollinators. At fine taxonomic scale, we found that for both pollinator and parasites, species were generally specific to a given fig host. Moreover, the phylogenies of the non-pollinators are largely congruent with those of the pollinators, suggesting the predominance of strict-sense co-evolution on shared host fig species. The implications of these findings and opportunities for future research are discussed.     

高榕雌花期传粉榕小蜂和欺骗性小蜂的繁殖特点

榕树及其专一性传粉榕小蜂组成了动植物界最为经典的协同进化关系,传粉榕小蜂演化出欺骗性是非常罕见的。在雌雄同株的高榕隐头果内,共存着一种传粉榕小蜂Eupristina altissima和一种欺骗性的小蜂Eupristina sp.,两种小蜂在雌花期进入隐头果内繁殖,但有不同的繁殖特点。对比研究了两种小蜂从成虫羽化到产卵和传粉这个阶段的雌蜂个体大小、孕卵量及繁殖差异,结果表明:羽化期两种雌蜂的平均个体小,经飞行小个体的雌蜂易死亡,大个体雌蜂到达接受树,但通过苞片通道,一些个体较大的传粉榕小蜂被夹死导致进入果腔的雌蜂相对小,而欺骗性小蜂易通过苞片以至进入果腔的雌蜂个体较大。两种未产卵雌蜂均表现为个体大者孕卵量较多,但两种雌蜂的平均孕卵量没有差异。即使有充足雌花资源产卵,两种雌蜂均未产完所有卵,产卵后两种雌蜂卵巢中的卵量均显著减少,遗留下的卵量两种小蜂间没有差异。传粉榕小蜂只有部分个体传完所携带花粉,并表现为传粉越成功的雌蜂,产卵越多。存在种内竞争时,两种小蜂的产卵量均减少,传粉榕小蜂的传粉效率也降低。在种间竞争背景下,欺骗性小蜂产卵更成功,传粉榕小蜂的产卵和传粉量均受到极大抑制。研究结果说明雌花期隐头果内传粉榕小蜂只适量利用雌花资源产卵繁殖后代,更有效地传粉繁殖榕树种子,这可能是维持榕-蜂互惠系统稳定共存的重要机制之一;欺骗者稳定存在需降低与传粉者的直接竞争,而欺骗者和传粉者分散在不同果内,甚至是不同的树上繁殖是理想的繁殖策略。     

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.     

Molecular phylogeny of fig wasp pollinators (Agaonidae, Hymenoptera) of Ficus section Galoglychia

The obligate mutualism between fig trees and their fig wasp pollinators, together with the general tendency for each host species to be pollinated by one fig wasp species, led to the hypothesis that these two lineages have cospeciated. The pollinators of African figs of section Galoglychia form a diverse group of genera whose species seem to be less constrained to a specific host than other pollinating fig wasp genera. Various authors have suggested remarkably different phylogenetic relationships between the seven genera associated with section Galoglychia. These uncertainties concerning the classification make it difficult to understand the historical patterns of association between these wasps and their hosts. The phylogenetic tree for the pollinators was reconstructed with 28S, COI and ITS2 DNA sequence data and compared with morphological classification of the hosts. Pollinator genera were monophyletic in all analyses. However, the relative position of some genera remains unresolved. Investigation of host−fig association suggests that there have been frequent host jumps between host subsections. This indicates that cospeciation between fig trees and fig wasps is not as stringent as previously assumed. In addition, pollinators of the genus Alfonsiella associated with three host figs (Ficus craterostoma, F. stuhlmannii and F. petersii) are morphologically very similar in South Africa. We investigated the possibility that these pollinators form a complex of species with host‐based genetic differentiation. Molecular analyses supported the distinction of the pollinator of F. craterostoma as a good species, but the pollinators of F. stuhlmannii and F. petersii clustered within the same clade, suggesting that these two host species share a single pollinator, Alfonsiella binghami. Based on both molecular data and morphological re‐evaluation, a new Alfonsiella species is described, Alfonsiella pipithiensis sp. nov., which is the pollinator of F. craterostoma in southern Africa. A key to both females and males of all described species of Alfonsiella is provided.     

薜荔榕小蜂对薜荔和爱玉子雌花期榕果挥发物的行为反应

薜荔和爱玉子均属雌雄异株桑科榕属植物,两者互为原变种与变种的关系,分别与薜荔传粉小蜂和爱玉子传粉小蜂(二者互为隐存种)建立了专性共生关系,榕树榕果挥发物在维系传粉小蜂与其寄主的共生关系上起着重要作用。利用Y型嗅觉仪测定薜荔榕小蜂(薜荔和爱玉子的传粉小蜂)对薜荔和爱玉子雌花期榕果挥发物的行为反应。结果表明:(1)雌花期果型的大小对薜荔榕小蜂行为反应无显著影响,薜荔大、小果型雌花期雌(雄)榕果挥发物对其传粉小蜂均具有强烈的吸引作用;(2)榕果挥发物浓度影响薜荔榕小蜂行为反应,薜荔、爱玉子雌花期雌(雄)榕果挥发物对其传粉小蜂的吸引作用均可能存在阈值反应,即榕果挥发物浓度未超过阈值时,雌花期榕果挥发物对传粉小蜂的吸引作用与挥发物浓度成正相关关系,而一旦超过阈值,榕果挥发物对传粉蜂的吸引作用显著下降,表明寄主榕果挥发物浓度影响传粉小蜂的寄主定位;(3)薜荔传粉小蜂对低浓度爱玉子雌花期雌(雄)榕果挥发物、爱玉子传粉小蜂对低浓度薜荔雌花期雌(雄)榕果挥发物均既无趋向也无驱避行为;薜荔传粉小蜂对高浓度的爱玉子雌花期雌(雄)榕果挥发物表现为显著的驱避行为,而爱玉子传粉小蜂对高浓度薜荔雌(雄)雌花期榕果挥发物表现为显著的趋向行为,因此,薜荔传粉小蜂与爱玉子传粉小蜂存在寄主专一性不对称现象,爱玉子传粉小蜂进入薜荔雌(雄)果内传粉或产卵的可能性较大,而福州地区的薜荔传粉小蜂可能难以进入爱玉子雌(雄)果内传粉或产卵。本研究结果将为榕-蜂共生体系的化学生态学理论研究以及爱玉子栽培提供科学依据。     

Pollination and parasitism in functionally dioecious figs

Fig wasps (Agaonidae: Hymenoptera) are seed predators and their interactions with Ficus species (Moraceae) range from mutualism to parasitism. Recently considerable attention has been paid to conflicts of interest between the mutualists and how they are resolved in monoecious fig species. However, despite the fact that different conflicts can arise, little is known about the factors that influence the persistence of the mutualism in functionally dioecious Ficus. We studied the fig pollinator mutualism in 14 functionally dioecious fig species and one monoecious species from tropical lowland rainforests near Madang, Papua New Guinea. Observations and experiments suggest that (i) pollinating wasps are monophagous and attracted to a particular host species; (ii) pollinating and non-pollinating wasps are equally attracted to gall (male) figs and seed (female) figs in functionally dioecious species; (iii) differing style lengths between gall figs and seed figs may explain why pollinators do not develop in the latter; (iv) negative density dependence may stabilize the interaction between pollinating wasps and their parasitoids; and (v) seed figs may reduce the search efficiency of non-pollinators. This increased pollinator production without a corresponding decrease in seed production could provide an advantage for dioecy in conditions where pollinators are limiting.     

Figs,pollinators, and parasites: A longitudinal study of the effects of nematode infection on fig wasp fitness

Mutualisms are interactions between two species in which the fitnesses of both symbionts benefit from the relationship. Although examples of mutualism are ubiquitous in nature, the ecology, evolution, and stability of mutualism has rarely been studied in the broader, multi-species community context in which they occur. The pollination mutualism between figs and fig wasps provides an excellent model system for investigating interactions between obligate mutualists and antagonists. Compared to the community of non-pollinating fig wasps that develop within fig inflorescences at the expense of fig seeds and pollinators, consequences of interactions between female pollinating wasps and their host-specialist nematode parasites is much less well understood. Here we focus on a tri-partite system comprised of a fig (Ficus petiolaris), pollinating wasp (Pegoscapus sp.), and nematode (Parasitodiplogaster sp.), investigating geographical variation in the incidence of attack and mechanisms through which nematodes may limit the fitness of their wasp hosts at successive life history stages. Observational data reveals that nematodes are ubiquitous across their host range in Baja California, Mexico; that the incidence of nematode infection varies across seasons within- and between locations, and that infected pollinators are sometimes associated with fitness declines through reduced offspring production. We find that moderate levels of infection (1–9 juvenile nematodes per host) are well tolerated by pollinator wasps whereas higher infection levels (≥10 nematodes per host) are correlated with a significant reduction in wasp lifespan and dispersal success. This overexploitation, however, is estimated to occur in only 2.8% of wasps in each generation. The result that nematode infection appears to be largely benign – and the unexpected finding that nematodes frequently infect non-pollinating wasps – highlight gaps in our knowledge of pollinator-Parasitodiplogaster interactions and suggest previously unappreciated ways in which this nematode may influence fig and pollinator fitness, mutualism persistence, and non-pollinator community dynamics.     

Can chemical signals,responsible for mutualistic partner encounter,promote the specific exploitation of nursery pollination mutualisms? – The case of figs and fig wasps

In nursery pollination mutualisms, where pollinators reproduce within the inflorescence they pollinate, floral scents often play a major role in advertizing host location and rewards for the pollinator. However, chemical messages emitted by the plant that are responsible for the encounter of mutualist partners can also be used by parasites of these mutualisms to locate their host. Each species of Ficus (Moraceae) is involved in an obligatory nursery pollination mutualism with usually one pollinating fig wasp (Hymenoptera: Chalcidoidea: Agaonidae). In this interaction, volatile compounds emitted by receptive figs are responsible for the attraction of their specific pollinator. However, a large and diverse community of non-pollinating chalcidoid wasps can also parasitize this mutualism. We investigated whether the chemical message emitted by figs to attract their pollinator can promote the host specificity of non-pollinating fig wasps. We analysed the volatile compounds emitted by receptive figs of three sympatric Ficus species, namely, Ficus hispida L., Ficus racemosa L., and Ficus tinctoria G. Forster, and tested the attraction of the pollinator of F. hispida ( Ceratosolen solmsi marchali Mayr), and of one species of non-pollinating fig wasp [ Philotrypesis pilosa Mayr (Hymenoptera: Chalcidoidea: Pteromalidae)] to scents emitted by receptive figs of these three Ficus species. Analysis of the volatile compounds emitted by receptive figs revealed that the three Ficus species could be clearly distinguished by their chemical composition. Behavioural bioassays performed in a Y-tube olfactometer showed that both pollinator and parasite were attracted only by the specific odour of F. hispida . These results suggest that the use by non-pollinating fig wasps of a specific chemical message produced by figs could limit host shifts by non-pollinating fig wasps.