Dioecious Fig Research Articles

Spatial genetic structure of Ficus superba (Moraceae) in mainland and insular Singapore

Monoecious Ficus L. (Moraceae) species have putatively effective long-distance pollen dispersal and low population densities. The lack of spatially defined populations and the assumption of high gene flow led to the dearth of work on the Spatial Genetic Structure (SGS) of monoecious species. Furthermore, as only forest or inland species were studied, the effects of landscape heterogeneity and discontinuous habitats have been overlooked. To address this, Ficus superba (Miq.) Miq., a monoecious spatially aggregated coastal and insular species from Singapore, was studied to ascertain if population homogenisation could result from pollen flow even when the assumptions of spatial and landscape homogeneity were violated. Individuals were genotyped using dominant Amplified Fragment Length Polymorphism (AFLP) markers. Bayesian clustering software and Principal Component Analysis (PCA) were used to test for population genetic structure. SGS analyses and Mantel’s Tests were performed to test for the presence of significant fine-scale SGS and Isolation By Distance (IBD). Significant population genetic structure and SGS were found, with one mainland population more differentiated from the remaining insular and mainland populations. It is hypothesised that the spatial aggregation and landscape heterogeneity significantly distort gene flow through aggregated seed dispersal and greater impedance to pollen flow over land than sea. This calls into question the supposed dichotomy in gene flow characteristics of monoecious versus dioecious figs attributed to pollinator behaviour.

Evolution of Wolbachia reproductive and nutritional mutualism: insights from the genomes of two novel strains that double infect the pollinator of dioecious Ficus hirta.

Wolbachia is a genus of maternally inherited endosymbionts that can affect reproduction of their hosts and influence metabolic processes. The pollinator, Valisia javana, is common in the male syconium of the dioecious fig Ficus hirta. Based on a high-quality chromosome-level V. javana genome with PacBio long-read and Illumina short-read sequencing, we discovered a sizeable proportion of Wolbachia sequences and used these to assemble two novel Wolbachia strains belonging to supergroup A. We explored its phylogenetic relationship with described Wolbachia strains based on MLST sequences and the possibility of induction of CI (cytoplasmic incompatibility) in this strain by examining the presence of cif genes known to be responsible for CI in other insects. We also identified mobile genetic elements including prophages and insertion sequences, genes related to biotin synthesis and metabolism. A total of two prophages and 256 insertion sequences were found. The prophage WOjav1 is cryptic (structure incomplete) and WOjav2 is relatively intact. IS5 is the dominant transposon family. At least three pairs of type I cif genes with three copies were found which may cause strong CI although this needs experimental verification; we also considered possible nutritional effects of the Wolbachia by identifying genes related to biotin production, absorption and metabolism. This study provides a resource for further studies of Wolbachia-pollinator-host plant interactions.

Pollinator sharing and hybridization in a pair of dioecious figs sheds light on the pathways to speciation.

The dynamics and processes underlying the codiversification of plant-pollinator interactions are of great interest to researchers of biodiversity and evolution. Cospeciation is generally considered a key process driving the diversity of figs and their pollinating wasps. Groups of closely related figs pollinated by separate wasps occur frequently and represent excellent opportunities to study ongoing diversification in this textbook mutualism. We study two closely related sympatric dioecious figs (Ficus heterostyla and Ficus squamosa) in Xishuangbanna, southwest China, and aim to document what is likely to be the final stages of speciation between these species using a combination of trait data and experimental manipulation. Volatile profiles at the receptive phase, crucial for attracting pollinators, were analyzed. In total, 37 and 29 volatile compounds were identified from receptive F. heterostyla and F. squamosa figs, respectively. Despite significant interspecific dissimilarity, 25 compounds were shared. Ovipositor lengths lie well within range required for access to heterospecific ovules, facilitating hybridization. Cross introduction of wasps into figs was conducted and hybrid seeds were generated for all donor/recipient combinations. F. heterostyla wasps produce adult offspring in F. squamosa figs. While F. squamosa wasps induce gall development in F. heterostyla figs and their offspring fail to mature in synchrony with their novel host. We record limited geographic barriers, minimal volatile dissimilarity, compatible morphology, complementary reproductive phenologies, and the production of hybrid seeds and wasp offspring. These findings suggest ongoing wasp specialization and reproductive isolation, potentially applicable to other related fig species.

The genetic structuring in pollinating wasps of Ficus hispida in continental Asia.

The interaction between figs and fig wasps provides a striking example of obligate brood site pollination mutualism. Monoecious figs, constituting independent radiations in each tropical biome, are present in significant proportions worldwide, but in continental Asia, dioecious figs have diverged into various niches, making the region's assemblage remarkably diverse. However, the reproductive success of figs and fig wasps largely depends on the fig wasp dispersal process. Monoecious fig pollinators in continental Asian tropical rain forests exhibit high gene flow of the plant, while many dioecious fig pollinators have a more restricted gene flow. However, there are limited studies on the genetic structure of dioecious Ficus pollinators that pollinate figs with intermediate gene flow. Here, we used molecular methods to investigate the genetic structure of pollinating wasps of the widely distributed dioecious Ficus hispida in China and Southeast Asia. Sequence data from two gene regions were used: the mitochondrial protein-coding gene cytochrome c oxidase subunit I (COI) and the nuclear 28S genes. Both molecular and morphological results support two fig wasp species at our sampling sites. Our findings suggest that for widely sympatric Ficus species in continental Asia, monoecious figs presenting long gene glow have the fewest fig wasp species, followed by dioecious figs presenting intermediate gene flow, and dioecious figs presenting local gene flow have the most fig wasp species.

Enhanced and asymmetric signatures of hybridization at climatic margins: Evidence from closely related dioecious fig species

Hybridization plays a significant role in biological evolution. However, it is not clear whether ecological contingency differentially influences likelihood of hybridization, particularly at ecological margins where parental species may exhibit reduced fitnesses. Moreover, it is unknown whether future ecosystem change will increase the prevalence of hybridization. Ficus heterostyla and F. squamosa are closely related species co-distributed from southern Thailand to southwest China where hybridization, yielding viable seeds, has been documented. As a robust test of ecological factors driving hybridization, we investigated spatial hybridization signatures based on nuclear microsatellites from extensive population sampling across a widespread contact range. Both species showed high population differentiation and strong patterns of isolation by distance. Admixture estimates exposed asymmetric interspecific gene flow. Signatures of hybridization increase significantly towards higher latitude zones, peaking at the northern climatic margins. Geographic variation in reproductive phenology combined with ecologically challenging marginal habitats may promote this phenomenon. Our work is a first systematic evaluation of such patterns in a comprehensive, latitudinally-based clinal context, and indicates that tendency to hybridize appears strongly influenced by environmental conditions. Moreover, that future climate change scenarios will likely alter and possibly augment cases of hybridization at ecosystem scales.

East‒West genetic differentiation across the Indo-Burma hotspot: evidence from two closely related dioecious figs

BackgroundUnderstanding biodiversity patterns and their underlying mechanisms is of interest to ecologists, biogeographers and conservationists and is critically important for conservation efforts. The Indo-Burma hotspot features high species diversity and endemism, yet it also faces significant threats and biodiversity losses; however, few studies have explored the genetic structure and underlying mechanisms of Indo-Burmese species. Here, we conducted a comparative phylogeographic analysis of two closely related dioecious Ficus species, F. hispida and F. heterostyla, based on wide and intensive population sampling across Indo-Burma ranges, using chloroplast (psbA-trnH, trnS-trnG) and nuclear microsatellite (nSSR) markers, as well as ecological niche modeling.ResultsThe results indicated large numbers of population-specific cpDNA haplotypes and nSSR alleles in the two species. F. hispida showed slightly higher chloroplast diversity but lower nuclear diversity than F. heterostyla. Low-altitude mountainous areas of northern Indo-Burma were revealed to have high genetic diversity and high habitat suitability, suggesting potential climate refugia and conservation priority areas. Strong phylogeographic structure and a marked east‒west differentiation pattern were observed in both species, due to the interactions between biotic and abiotic factors. Interspecific dissimilarities at fine-scale genetic structure and asynchronized historical dynamics of east‒west differentiation between species were also detected, which were attributed to different species-specific traits.ConclusionsWe confirm hypothesized predictions that interactions between biotic and abiotic factors largely determine the patterns of genetic diversity and phylogeographic structure of Indo-Burmese plants. The east‒west genetic differentiation pattern observed in two targeted figs can be generalized to some other Indo-Burmese plants. The results and findings of this work will contribute to the conservation of Indo-Burmese biodiversity and facilitate targeted conservation efforts for different species.

Mediation of a Mutualistic Conflict for Pollination via Fig Phenology and Odor Recognition between Ficus and Fig Wasp.

The vegetative and reproductive growth of plants provide the basic tempo for an ecosystem, and when species are interdependent, phenology becomes crucial to regulating the quantity and quality of the interactions. In plant–insect interactions, the plants signal the beginning of their reproductive period with visual and chemical cues; however, in the case of Ficus mutualism, the cues are strictly chemical. The volatile organic compounds emitted by a fig species are a unique, specific blend that provides a signal to mutualistic wasps that the figs are receptive for pollination. In this study, we studied both the phenological pattern of Ficus septica in Central Taiwan and its emissions of volatile compounds at receptivity. This dioecious fig species displays a pattern of continuous vegetative and reproductive production all through the year with a decrease in winter. In parallel, the odor blends emitted by male and female trees are similar but with seasonal variations; these are minimal during winter and increase with the size of the wasp population during the favorable season. In addition, the pollinating females cannot distinguish between the male and female summer odor blends. The link between odor similarity, pollinators and intersexual conflict is discussed.

Pollinator sharing, copollination, and speciation by host shifting among six closely related dioecious fig species

The obligate pollination mutualism between figs (Ficus, Moraceae) and pollinator wasps (Agaonidae, Hymenoptera) is a classic example of cospeciation. However, examples of phylogenetic incongruencies between figs and their pollinators suggest that pollinators may speciate by host shifting. To investigate the mechanism of speciation by host shifting, we examined the phylogenetic relationships and population genetic structures of six closely related fig species and their pollinators from southern China and Taiwan-Ryukyu islands using various molecular markers. The results revealed 1) an extraordinary case of pollinator sharing, in which five distinct fig species share a single pollinator species in southern China; 2) two types of copollination, namely, sympatric copollination by pollinator duplication or pollinator migration, and allopatric copollination by host migration and new pollinator acquisition; 3) fig species from southern China have colonized Taiwan repeatedly and one of these events has been followed by host shifting, reestablishment of host specificity, and pollinator speciation, in order. Based on our results, we propose a model for pollinator speciation by host shifting in which the reestablishment of host-specificity plays a central role in the speciation process. These findings provide important insights into understanding the mechanisms underlying pollinator speciation and host specificity in obligate pollination mutualism.

Association of Fig Pollinating Wasps and Fig Nematodes inside Male and Female Figs of a Dioecious Fig Tree in Sumatra, Indonesia

Simple SummaryIt has been known that fig pollinating wasps can transfer nematodes when they enter receptive figs to deposit their eggs (male figs in male trees) and pollinate the flowers (female figs in female trees) of a dioecious fig tree. However, the fate of nematodes transferred into female figs was unknown, since the pollinating wasps that enter female figs cannot reproduce. This study examined whether the nematodes transferred by pollinating wasps into female figs of Ficus hispida could develop and reproduce in the same way as in male figs. Three species of nematodes were found to develop within the male and female figs of F. hispida, with populations peaking at about the same time for both sexes of figs. Our findings showed that the female figs could support the growth and reproduction of the three nematodes; however, there was no pollinator offspring to transfer the nematodes out of the figs. The results provide a better understanding of the development of nematodes in male and female figs of a dioecious fig tree, which may also influence the biodiversity of the tropical ecosystem.Nematodes can grow within the inflorescences of many fig trees (Ficus spp., Moraceae); however, the feeding behaviour of most nematodes is not known. Fig pollinating wasps (Hymenoptera: Agaonidae) transfer nematodes into young figs upon the wasps’ entry into the figs to deposit their eggs. Most Asian fig trees, however, are functionally dioecious, and the pollinating wasps that enter female figs are unable to reproduce. They fail to produce the offspring required to carry the new generations of nematodes. We examined whether female figs of F. hispida can nonetheless support the development of phoretic nematode populations. Nematodes were extracted from male and female figs sampled in Sumatra, Indonesia, to compare the growth of their populations within the figs. We found three species of nematodes that grew within figs of male and female trees of F. hispida: Ficophagus cf. centerae (Aphelenchoididae), Martininema baculum (Aphelenchoididae) and Caenorhabditis sp (Rhabditidae). The latter species (Caenorhabditis sp.) has never been reported to be associated with F. hispida before. Nematode populations peaked at around 120–140 individuals in both sexes of figs, at the time when a succeeding generation of adult fig wasps appeared within male figs. The female figs could support the growth and reproduction of the three nematodes species; however, the absence of vectors meant that female figs remained as traps from which there could be no escape.

Asymmetric sharing of pollinator fig wasps between two sympatric dioecious fig trees: a reflection of supply and demand or differences in the size of their figs?

BackgroundHost specificity among pollinator fig wasps (Agaonidae) depends on host plant specific volatile cues, but fig wasps must also pass through a narrow physical barrier (the ostiole) if they are to pollinate and oviposit. Across South East Asia the dioecious shrub Ficus hirta is associated with at least ten pollinator species allied to Valisia javana. Ficus triloba has a single recorded pollinator, Valisia esquirolianae. Receptive figs of F. hirta are usually much smaller than those of F. triloba, but at a mainland site where F. hirta has atypically large figs we identified both V. esquirolianae and V. javana from both Ficus species using COI and ITS2 sequencing. To investigate whether this host overlap was exceptional we reared fig wasps from the two trees elsewhere and recorded features that may facilitate host transfer between them, including attractant volatiles, reproductive phenology and the sizes of their figs and fig wasps.ResultsThe two Ficus species were found to support both Valisia species at several of the sites, suggesting that the differences we detected in volatile profiles, ostiole sizes and pollinator head sizes are not strict barriers to host sharing. Valisia javana colonised F. triloba more frequently than V. esquirolianae colonised F. hirta.ConclusionsThis asymmetric sharing of pollinators may reflect the relative abundance of the two species of fig wasps and differences in host reproductive phenology. Asynchronous flowering of individual F. hirta may favor local retention of pollinators, in contrast to the tree-wide synchrony of F. triloba figs, which can generate local shortages of V. esquirolianae. If the pollinator sharing by male figs of F. triloba and F. hirta also occurs in female figs then this could result in gene flow between them.

More examples of breakdown the 1:1 partner specificity between figs and fig wasps

BackgroundThe obligate mutualism between fig trees (Ficus, Moraceae) and pollinating fig wasps (Agaonidae) is a model system for studying co-evolution due to its perceived extreme specificity, but recent studies have reported a number of examples of trees pollinated by more than one fig wasp or sharing pollinators with other trees. This will make the potential of pollen flow between species and hybridization more likely though only few fig hybrids in nature have been found. We reared pollinator fig wasps from figs of 13 Chinese fig tree species and established their identity using genetic methods in order to investigate the extent to which they were supporting more than one species of pollinator (co-pollinator).ResultsOur results showed (1) pollinator sharing was frequent among closely-related dioecious species (where pollinator offspring and seeds develop on different trees); (2) that where two pollinator species were developing in figs of one host species there was usually one fig wasp with prominent rate than the other. An exception was F. triloba, where its two pollinators were equally abundant; (3) the extent of co-pollinator within one fig species is related to the dispersal ability of them which is stronger in dioecious figs, especially in small species.ConclusionsOur results gave more examples to the breakdown of extreme specificity, which suggest that host expansion events where pollinators reproduce in figs other than those of their usual hosts are not uncommon among fig wasps associated with dioecious hosts. Because closely related trees typically have closely related pollinators that have a very similar appearance, the extent of pollinator-sharing has probably been underestimated. Any pollinators that enter female figs carrying heterospecific pollen could potentially generate hybrid seed, and the extent of hybridization and its significance may also have been underestimated.

Adaptation of Fig Wasps (Agaodinae) to Their Host Revealed by Large-Scale Transcriptomic Data.

Simple SummaryResearch on fig wasps has made a considerable contribution to the understanding of insect–plant interactions. However, the molecular mechanisms underlying fig wasp host specificity are poorly understood. This study reports on a relatively large-scale transcriptomic dataset of 25 fig wasp species. We outline potential genetic mechanisms underlying the specific host adaptation by investigating changes in a gene family, in evolutionary rates, and in genes under positive selection. The transcriptome datasets reported here (1) provide new insights into the evolutionary diversification and host specificity of fig wasps and (2) contribute to a growing dataset on fig wasp genomics.Figs and fig wasps are highly species-specific and comprise a model system for studying co-evolution and co-speciation. The evolutionary relationships and molecular adaptations of fig wasps to their fig hosts are poorly understood, and this is in part due to limited sequence data. Here, we present large-scale transcriptomic datasets of 25 fig wasp species with the aim of uncovering the genetic basis for host specificity. Our phylogenetic results support the monophyly of all genera associated with dioecious figs, and two genera associated with monoecious figs, Eupristina and Platyscapa, were revealed to be close relatives. We identified gene loss and gain, potentially rapidly evolving genes, and genes under positive selection. Potentially functional changes were documented and we hypothesize as to how these may determine host specificity. Overall, our study provides new insights into the evolutionary diversification of fig wasps and contributes to our understanding of adaptation in this group.

The plastid genome of winter cropping plants Ficus tinctoria (Moraceae)

Ficus tinctoria subsp. gibbosa (Blume) Corner is a hemiepiphytic dioecious fig species of the genus Ficus in the family Moraceae. To better determine its phylogenetic location with respect to the other Ficus species, the complete plastid genome of F. tinctoria was sequenced. The whole plastome is 160,342 bp in length, consisting of a pair of inverted repeat (IR) regions of 25,859 bp, one large single-copy (LSC) region of 88,526 bp, and one small single-copy (SSC) region of 20,098 bp. The overall GC content of the whole plastome is 35.9%. Further, maximum likelihood (ML) phylogenetic analyze was conducted using 23 complete fig plastomes, which support close relationships among F. tinctoria, F. heteropleura, F. obscura, and F. deltoidea.

Differentiation during fig ontogeny suggests opposing selection by mutualists.

Dioecy allows separation of female and male functions and therefore facilitates separate co‐evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower‐stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male (“gall”) figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female (“seed”) figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.

Fruiting phenology and nutrient content variation among sympatric figs and the ecological correlates

BackgroundFigs are key resources for tropical frugivores and display unique fruiting patterns. While monoecious figs support both seeds and wasp rearing, dioecious plants perform the tasks separately and produce seeded figs in smaller asynchronous crops. Thus dioecious females, compared to monoecious figs, may afford to invest more efforts to maximize seediness, or increase fruit pulp, water content, and nutrient rewards to attract frugivores for better seed dispersal. Yet size variation among and within fig species in either breeding system may lead to complicated resource allocation. We assessed fruiting phenology, measured fig morphological traits, and analyzed fig nutrient contents of the monoecious Ficus caulocarpa and F. subpisocarpa and the dioecious F. ampelas and F. irisana in a sympatric tropical forest to investigate species differences and size effects on fig functional traits and their ecological correlates.ResultsAll four species fruited nearly year-round. Monoecious figs’ inter-tree asynchronous crops had high peak mature crop sizes over much shorter fruiting periods than dioecious figs. Among trees, F. subpisocarpa and F. irisana were greater in fig-size and size variation, F. caulocarpa and F. ampelas comparatively displayed large variation in fig compositions. As fig size increased, water contents gradually increased in large-fig species, but seediness with a decreasing trend in small-fig species. Dioecious figs had lower pulp-seed ratio but tended to have higher water contents than monoecious figs, particularly within a similar size range. Dioecious figs also had higher carbohydrates, whereas monoecious figs contained higher fiber and lipid contents.ConclusionsOur study revealed species differences in certain fig functional traits that were correlated with fig size or their breeding systems, with substantial inter-tree variation. This partially supported the predictions regarding their fruiting strategies of aiding seed dispersal by frugivores, yet suggests a fruiting plasticity of individual trees subject to environmental constraints and their biotic interactions.

Preference of an insular flying fox for seed figs enhances seed dispersal of a dioecious species

AbstractInteractions among multiple species form complex networks of interdependences and are considered primary factors in the generation and maintenance of biodiversity. Pteropodid bats are keystone species that provide important ecosystem services of pollination and seed dispersal in the tropics and subtropics. In this study, we investigated the utilization and preference of food resources by the insular frugivorous flying fox Pteropus dasymallus. We found that fig species constituted the major portion of the diet of the flying fox (94.6%). When foraging, the flying fox preferred seed figs from female trees over gall figs from male trees in functionally dioecious fig species. Germination experiments showed a significantly higher percentage of germination for fig seeds in feces than those from pellets and ripe figs (feces: 80.2%, pellets: 23.4%, ripe figs: 32.9%). Considering the active selection of seed figs and avoidance of gall figs by foraging flying foxes, we suggest that the abundance of seed figs accurately represents food availability for dioecy. This preference for seed figs or viable seeds can effectively promote the survival of pollinating wasps and might reinforce the evolution of dioecism in figs. In addition, the effects of gut passage on seed germination, in combination with the capacity of flying foxes to travel long distances, may substantially contribute to the efficiency of flying foxes as seed dispersers.

Style length variation in male and female figs: development, inheritance, and control of pollinator oviposition

AbstractFig trees (Ficus spp., Moraceae) depend on female fig wasps to transport their pollen and as a reward provide nutrition for pollinator fig wasp larvae. Most pollinators are host specific, but natural plant hybrids occur if atypical hosts are pollinated. Female fig wasps lay their eggs into ovaries of female flowers in receptive figs by inserting their ovipositors through the styles, and relative style and ovipositor lengths are believed to largely determine their ability to oviposit. In dioecious fig trees, flowers in receptive male figs have short styles and support larval development, whereas flowers in receptive female figs have long styles and only develop into seeds. Using the dioecious fig tree species Ficus montana Burm. f. and Ficus asperifolia Miq., we recorded the comparative ontogeny of style lengths to determine whether style growth in the two sexes is coordinated with the attraction of pollinators, and how maximum style lengths relate to the ovipositor lengths of their pollinators. F1 hybrids between these species produce viable seeds, but no pollinator offspring. We examined style lengths in F1s and backcrosses, relative to those of their parents, and whether coordination of style growth with pollinator attraction is disrupted. The ovipositor of Kradibia tentacularis (Grandi) (Hymenoptera: Agaonidae), the pollinator of F. montana, could reach some of the ovaries in female figs, but fails to lay eggs there. Styles in male F1 figs were intermediate in length between those of the two parents, but in female F1 figs styles grew longer than in either parent. Maximum style lengths in F1s were partially decoupled from receptivity, especially in female figs. Our results illustrate how timing of stigmal growth is coordinated with pollinator attraction, and that this coordination can be disrupted in hybrid individuals.

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.

Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa.

Hybridization and insect pollination are widely believed to increase rates of plant diversification. The extreme diversity of figs (Ficus) and their obligate pollinators, fig wasps (Agaonidae), provides an opportunity to examine the possible role of pollinator-mediated hybridization in plant diversification. Increasing evidence suggests that pollinator sharing and hybridization occurs among fig taxa, despite relatively strict coevolution with the pollinating wasp. Using five sympatric dioecious fig taxa and their pollinators, we examine the degree of pollinator sharing and inter-taxa gene flow. We experimentally test pollinator preference for floral volatiles, the main host recognition signal, from different figs. All five fig taxa shared pollinators with other taxa, and gene flow occurred between fig taxa within and between sections. Floral volatiles of each taxon attracted more than one pollinator species. Floral volatiles were more similar between closely related figs, which experienced higher levels of pollinator sharing and inter-taxa gene flow. This study demonstrates that pollinator sharing and inter-taxa gene flow occurs among closely related sympatric dioecious fig taxa and that pollinators choose the floral volatiles of multiple fig taxa. The implications of pollinator sharing and inter-taxa gene flow on diversification, occurring even in this highly specialized obligate pollination system, require further study.

How to be a dioecious fig: Chemical mimicry between sexes matters only when both sexes flower synchronously.

In nursery pollination mutualisms, which are usually obligate interactions, olfactory attraction of pollinators by floral volatile organic compounds (VOCs) is the main step in guaranteeing partner encounter. However, mechanisms ensuring the evolutionary stability of dioecious fig–pollinator mutualisms, in which female fig trees engage in pollination by deceit resulting in zero reproductive success of pollinators that visit them, are poorly understood. In dioecious figs, individuals of each sex should be selected to produce odours that their pollinating wasps cannot distinguish, especially since pollinators have usually only one choice of a nursery during their lifetime. To test the hypothesis of intersexual chemical mimicry, VOCs emitted by pollen-receptive figs of seven dioecious species were compared using headspace collection and gas chromatography-mass spectrometry analysis. First, fig-flower scents varied significantly among species, allowing host-species recognition. Second, in species in which male and female figs are synchronous, intersexual VOC variation was not significant. However, in species where figs of both sexes flower asynchronously, intersexual variation of VOCs was detectable. Finally, with one exception, there was no sexual dimorphism in scent quantity. We show that there are two ways to use scent to be a dioecious fig based on differences in flowering synchrony between the sexes.