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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. Lay Summary: The coevolution of flowering plants and their animal pollinators is essential for fostering biodiversity. Exploring the dynamics and processes underlying plant–pollinator interactions is of evolutionary interest and critical for understanding biodiversity origins. Ficus, a diverse genus, is well-known for its species-specific relationships with pollinating wasps. Cospeciation plays an important role in the formation of fig and wasp diversity, as the reciprocal adaptations have led to the development of strong prezygotic barriers. Nevertheless, wasps exhibit much shorter generation times compared to figs, resulting in faster speciation rates. Often, fig complexes or closely related figs coevolve with distinct wasp species, representing the final step toward complete fig speciation and providing an excellent opportunity for studying ongoing mutualistic diversification. In such scenarios, heterospecific visitation of wasps may trigger interspecific pollination. Here, we examined reproductive isolation between two closely related figs, Ficus heterostyla and Ficus squamosa, through trait data and experimental manipulation. Floral volatiles emitted by receptive figs, which are crucial signals for attracting specific wasps, exhibited considerable overlap between these two fig species. The lengths of the wasp ovipositors were well within the range required for access to heterospecific ovules. Hybrid seeds were produced experimentally, with results showing that wasps of F. heterostyla reproduced in F. squamosa figs, while wasps of F. squamosa did not reproduce in F. heterostyla figs. Overall, heterospecific visitation decreased both fig and wasp fitness. Together with geographic barriers and complementary reproductive phenologies, these findings suggest that prezygotic isolation between F. heterostyla and F. squamosa may not yet be established. [ABSTRACT FROM AUTHOR]

1. Species interactions in tightly bound ecological mutualisms often feature highly specialised species' roles in which competitive exclusion may preclude multi‐species coexistence. Among the 800 fig (Ficus) species, it was originally considered that each was pollinated by their own wasp (Agaonidae). However, recent investigations show that this 'one‐to‐one' rule often breaks down, as fig species regularly host multiple agaonids but in ways suggesting that competitive processes still mediate biodiversity outcomes. 2. A phenological survey was conducted of the fig–fig wasp pair, Ficus microcarpa and its associated pollinating wasp, alongside its sister species, the cheating wasp, in Xishuangbanna, China. 3. Reproductive output underwent extreme seasonal variation. Seed and pollinator production fell markedly during cooler, drier months, although high levels of fig production continued. However, this resource was predominantly utilised by the cheater species, which offers no pollination services. Pollinators and cheaters rarely co‐occur, suggesting that temporal coexistence is constrained by competition for access to figs. 4. The overall findings indicate periodic rearrangements of mutualism dynamics, probably resulting from a strongly seasonal environment. Sympatric co‐occurrence may result from a window of opportunity for a functionally divergent agaonid, potentially due to constraints on the main pollinator in adapting to variable year‐round conditions that prevent competitive exclusion. [ABSTRACT FROM AUTHOR]

Floral scents are known as an olfactory signal for attracting pollinators, but why the flowers pollinated by highly specialised pollinators emit scents consisting of mixtures of many compounds and dominated by one or a few compounds is still poorly understood. We supposed that each (especially characteristic) chemical in floral scents may play a specific role in mediating pollinator behaviours and tested this supposition in a fig-fig wasp mutualism.Ficus curtipesis obligately pollinated by an undescribedEupristinaspecies. In the scent ofF.curtipesreceptive figs, over 50 compounds have been identified, and the scent is dominated by two compounds, 6-methyl-5-hepten-2-ol (OL) and 6-methyl-5-hepten-2-one (NE). We therefore tested the roles of the two major chemicals in mediating the pollinator behaviours. Our results show that OL and NE, respectively, act as a long-distance attractant and a fig-entry behaviour stimulant to the obligate pollinator wasp. Namely, OL attracts the wasps to the figs and NE guides the wasps into the figs. This finding on the work division of floral scent compounds partially explains the maintenance mechanism of the fig-fig wasp mutualism and the significance of the chemical diversity of floral scent in plant–pollinator interactions, especially in specialised pollination systems. [ABSTRACT FROM PUBLISHER]

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. [ABSTRACT FROM AUTHOR]

Pollinator fig wasps serve as useful empirical models for studies of sex ratio evolution because females adjust their offspring sex ratios in relation to the number of foundresses that share a fig. Placement of pollinator offspring within figs is not random and more centrally located flowers are more likely to support pollinator development. We compared components of fitness of female fig wasps developing in central and peripheral flowers and whether this influenced the sex ratios of their offspring. We used Ceratosolen solmsi marchali , a pollinator of the Asian dioecious fig tree, Ficus hispida . Mating frequency was determined from the number of mating holes in females' flowers. Most females mated once, but some had the opportunity to mate up to four times and multiple mating opportunities were more frequent among centrally located galls. Body size was not linked to flower location, although the females that mated most were significantly larger than others, and came from significantly larger galls. Females that had multiple mating opportunities produced more daughters but similar numbers of sons, resulting in more female-biased broods. These females are likely to have produced more offspring because of their larger size but may have also benefited from mating with more males. The results demonstrate that differences in the natal locations of foundresses can modify offspring sex ratios and obscure sex ratio adjustment in response to the number of foundresses sharing a fig. [ABSTRACT FROM AUTHOR]

Adult life spans of only one or two days characterise life cycles of the fig wasps (Agaonidae) that pollinate fig trees (Ficus spp., Moraceae). Selection is expected to favour traits that maximise the value of the timing of encounters between such mutualistic partners, and fig wasps are usually only attracted to their hosts by species- and developmental-stage specific volatiles released from figs at the time when they are ready to be entered, oviposited in and pollinated. We found that Ficus altissima is exceptional, because it has persistent tight-fitting bud covers that prevent its Eupristina altissima pollinator (and a second species of ‘cheater’ agaonid) from entering its figs for several days after they start to be attracted. We examined the consequences of delayed entry for the figs and fig wasps and tested whether delayed entry has been selected to increase adult longevity. We found that older pollinators produced fewer and smaller offspring, but seed production was more efficient. Pollinator offspring ratios also varied depending on the age of figs they entered. The two agaonids from F. altissima lived slightly longer than six congeners associated with typical figs, but this was explainable by their larger body sizes. Delayed entry generates reproductive costs, especially for the pollinator. This opens an interesting perspective on the coevolution of figs and their pollinators and on the nature of mutualistic interactions in general. [ABSTRACT FROM AUTHOR]

Plant odours are central for pollinator attraction. This is particularly true in obligate brood site pollination mutualisms. However, we know little about the evolution of olfactory signalling in these mutualisms. Here, we investigate geographic variation of floral odour in the obligate host-specific brood site pollination mutualism between Ficus hirta and its specialised pollinators. Floral scent samples from nine locations in China were collected using head-space adsorption and were analysed by gas chromatography-mass spectrometry. We evidence progressive geographic divergence of floral odours. The pattern of variation fits plant genetic structure for neutral genes but differs from pollinating insect structuring into species and populations. In our study system, the geographic variation of receptive floral odour presents a pattern that is not distinguishable from neutral drift. The variation is not canalised by the insects. We propose that this pattern characterises obligate brood site pollination mutualisms in which pollinators are host specific and dispersal of plant and insect is limited. Insects with their short generation times and large population sizes rapidly track any chance variation in host receptive inflorescence odours. Plants are the drivers and insects the followers. The source of the geographic variation in floral odours can be genetic or phenotypic in response to local conditions. Strict sense plant-insect co-evolution is not involved. In contrast, previous results on another Ficus -pollinating wasp association suggest that stabilising selection could be at work in more dispersive systems. • Here, we investigate the geographic variation of floral odour in the obligate host-specific brood site pollination mutualism between Ficus hirta and its specialised pollinators. We evidence that floral odours vary geographically in accordance to plant genetic variation but not to pollinating wasp structure, suggesting that plants are the drivers of geographic variation of floral odours in brood site pollination mutualisms. [ABSTRACT FROM AUTHOR]

Floral longevity reflects a balance between gains in pollinator visitation and the costs of flower maintenance. Because rewards to pollinators change over time, older flowers may be less attractive, reducing the value of extended longevity. Un-pollinated figs, the inflorescences of Ficus species, can remain receptive for long periods, but figs that are older when entered by their host-specific fig wasp pollinators produce fewer seeds and fig wasp offspring. Our field experiments with Ficus hispida, a dioecious fig tree, examined how the length of time that receptive figs have remained un-pollinated influences the behaviour and reproductive success of its short-lived fig wasp pollinator, Ceratosolen solmsi marchali. The results were consistent in three different seasons, and on male and female trees, although receptivity was greatly extended during colder months. Pollinators took longer to find the ostioles of older figs, and longer to penetrate them. They also became increasingly unwilling to enter figs as they aged, and increasing numbers of the wasps became trapped in the ostiolar bracts. Larger individuals were particularly unwilling to enter older figs, resulting in older figs being pollinated by smaller wasps. On female trees, where figs produce only seeds, seed production declined rapidly with fig age. On male trees, the numbers and size of fig wasp offspring declined, and a higher proportion were male. Older male figs are harder to enter, especially for larger individuals, and offer poorer quality oviposition opportunities. This study opens an interesting new perspective on the coevolution of figs and their pollinators, especially factors influencing pollinator body size and emphasises the subtleties of interactions between mutualists. [ABSTRACT FROM AUTHOR]

• In male figs agaonid wasps deposit a single pollen grain each time they oviposit. • Stigma shape and pollen transfer to the hypopygium ensure very precise pollination. • In female figs wasp behaviour is less precise than in male figs. • In female figs exposed stigmatic papillae and synstigma ensure efficient seed set. • Plant morphology stabilises the mutualism. Active pollination has evolved four times in brood site pollination mutualisms. When pollination is active, the pollinator's behaviour specifically evolves to ensure flower fertilisation. In functionally dioecious Ficus species, the male figs host pollinating wasp larvae, while wasps cannot breed in the female figs because the styles are longer than the wasp ovipositor. Here we investigate the dioecious Ficus hispida. We show that in male figs, every time the wasp has laid an egg into a pistillate flower, it removes one pollen grain from its pollen pockets and places it on the hypopygium. When the wasp inserts its ovipositor into the next flower, the pollen grain is deposited deep within the style. Each ovipositor insertion results in flower pollination and insect oviposition. Because of systematic pollination of the flowers into which the eggs are laid, the wasp larvae benefit from feeding on fertilised endosperm while no seed are produced. In female figs, after probing a flower, the wasp presents pollination behaviour only every five visits. However, if it does occur, this behaviour lasts longer than in male figs and results in the deposition of on average 10 pollen grains on the hypopygium. The exposed sticky papillae on the stigmatic surface collect pollen from the hypopygium and pollen tubes may grow to neighbouring stigmas, ensuring secondary dispersal and efficient ovule fertilisation. Overall, our study demonstrates that the floral morphology of male figs facilitates precise pollen deposition, beneficial for the wasp progeny, while the floral morphology of female figs compensates for wasp pollination behaviour that is not selected in those figs. We conclude that the morphology of the arena in which interactions with its pollinator are played out is the result of selection on the plant to maximize its male and female fitness. Incidentally, this morphology stabilises the mutualistic interaction. [ABSTRACT FROM AUTHOR]