Ability to gall: the ultimate basis of host specificity in fig wasps?

1. Fig trees (Ficus spp.) and their host‐specific pollinator fig wasps (Agaonidae) are partners in an obligate mutualism. Receptive phase figs release specific volatiles to attract their pollinators, and this is generally effective in preventing pollinator species from entering figs of the wrong hosts. 2. If entry is attempted into atypical host figs, then ostiole size and shape and style length may also prevent reproduction. In spite of these barriers, there is increasing evidence that fig wasps enter atypical hosts, and that this can result in hybrid seed and fig wasp offspring. 3. This study examines the basis of pollinator specificity in two dioecious fig species from different geographical areas. Kradibia tentacularis pollinates Ficus montana in Asia. Ficus asperifolia from East Africa is closely related but is pollinated by a different species of Kradibia. 4. In glasshouses, K. tentacularis was attracted to its normal host, F1s and backcrosses, but only rarely entered figs of F. asperifolia. Foundresses were able to lay eggs in hybrids, backcrosses, and F. asperifolia, although flower occupancy was lowest in F. asperifolia figs and intermediate in hybrids. 5. The fig wasp failed to reproduce in female F. montana, male F. asperifolia, and male F1s, and most but not all backcrosses to F. montana. This was a result of the failure to initiate gall production. 6. Host specificity in this fig wasp is strongly influenced by host volatiles, but the ability to gall may be the ultimate determinant of whether it can reproduce.     

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.     

The occurrence of fig wasps in the fruits of female gynodioecious fig trees

Fig trees are pollinated by wasp mutualists, whose larvae consume some of the plant's ovaries. Many fig species (350+) are gynodioecious, whereby pollinators generally develop in the figs of ‘male’ trees and seeds generally in the ‘females.’ Pollinators usually cannot reproduce in ‘female’ figs at all because their ovipositors cannot penetrate the long flower styles to gall the ovaries. Many non-pollinating fig wasp (NPFW) species also only reproduce in figs. These wasps can be either phytophagous gallers or parasites of other wasps. The lack of pollinators in female figs may thus constrain or benefit different NPFWs through host absence or relaxed competition. To determine the rates of wasp occurrence and abundance we surveyed 11 dioecious fig species on Hainan Island, China, and performed subsequent experiments with Ficus tinctoria subsp. gibbosa to identify the trophic relationships between NPFWs that enable development in female syconia. We found NPFWs naturally occurring in the females of Ficus auriculata, Ficus hainanensis and F. tinctoria subsp. gibbosa. Because pollinators occurred only in male syconia, when NPFWs also occurred in female syconia, overall there were more wasps in male than in female figs. Species occurrence concurred with experimental data, which showed that at least one phytophagous galler NPFW is essential to enable multiple wasp species to coexist within a female fig. Individuals of galler NPFW species present in both male and female figs of the same fig species were more abundant in females than in males, consistent with relaxed competition due to the absence of pollinator. However, these wasps replaced pollinators on a fewer than one-to-one basis, inferring that other unknown mechanisms prevent the widespread exploitation by wasps of female figs. Because some NPFW species may use the holes chewed by pollinator males to escape from their natal fig, we suggest that dispersal factors could be involved.     

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.     

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。     

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.     

Shift to mutualism in parasitic lineages of the fig/fig wasp interaction

The interaction between Ficus and their pollinating wasps (Chalcidoidea, Agaonidae) represents a striking example of mutualism. Figs also host numerous non-pollinating wasps belonging to other chalcidoid families. We show that six species of Ficus that are passively pollinated by the agaonid genus Waterstoniella also host specific wasps belonging to the chalcidoid genera Diaziella (Sycoecinae) and Lipothymus (Otitesellinae). Both belong to lineages that are considered as parasites of the fig/fig wasp mutualism. We show that these wasps are efficient pollinators of their hosts. Pollen counts on wasps of a species of Diaziella hosted by Ficus paracamptophylla show that Diaziella sp. transports more pollen than the associated pollinator when emerging from its natal fig. Further, the number of pollinated flowers in receptive figs is best explained by the number of Diaziella plus the number of Waterstoniella that had entered it. Figs that were colonised by Diaziella always produced seeds: Diaziella does not overexploit its host. Similarly, figs of Ficus consociata that were colonised solely by a species of Lipothymus produced as many seeds as figs that were colonised only by the legitimate pollinator Waterstoniella malayana . Diaziella sp. and Lipothymus sp. seem to pollinate their host fig as efficiently as do the associated agaonid wasps. Previous studies, on actively pollinated Ficus species, have found that internally ovipositing non-agaonid wasps are parasites of such Ficus species. Hence, mode of pollination of the legitimate pollinator conditions the outcome of the interaction between internally ovipositing parasites and their host.     

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.     

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.     

Interactions between pollinator and non‐pollinator fig wasps: correlations between their numbers can be misleading

Ficus and their species–specific pollinator fig wasps represent an obligate plant–insect mutualism, but figs also support a community of non‐pollinating fig wasps (NPFWs) that consist of phytophages and parasitoids or inquilines. We studied interactions between Kradibia tentacularis, the pollinator of a dioecious fig tree species Ficus montana, and an undescribed NPFW Sycoscapter sp. Members of Sycoscapter sp. oviposited 2–4 weeks after pollinator oviposition, when host larvae were present in the figs. No negative correlation was found between the numbers of the two wasp species emerging from figs in a semi‐natural population. However, in experiments where the numbers of pollinator foundresses entering a fig were controlled, Sycoscapter sp. significantly reduced the numbers of pollinator offspring. Consequently, it can be concluded that Sycoscapter sp. is a parasitoid of K. tentacularis (which may also feed on plant tissue). Sycoscapter females concentrate their oviposition in figs that contain more potential hosts, rendering invalid conclusions based on simple correlations of host and natural enemy numbers.     

Parasites and mutualism function: measuring enemy‐free space in a fig–pollinator symbiosis

Mutualisms involve cooperation between species and underpin several ecosystem functions. However, there is also conflict between mutualists, because their interests are not perfectly aligned. In addition, most mutualisms are exploited by parasites. Here, we study the interplay between cooperation, conflict and parasitism in the mutualism between fig trees and their pollinator wasps. Conflict occurs because each fig ovary can nurture either one seed or one pollinator offspring and, while fig trees benefit directly from seeds and pollinator offspring (pollen vectors), pollinators only benefit directly from pollinator offspring. The mechanism(s) of conflict resolution is debated, but must explain the widespread observation that pollinators develop in inner, and seeds in outer, layers of fig flowers. We recently suggested a role for non‐pollinating figs wasps (NPFWs) that are natural enemies or competitors of the pollinators and lay their eggs through the fig wall. Most NPFW offspring develop in outer and middle layer flowers, suggesting that inner flowers provide enemy‐free space for pollinator offspring. Here, we test the hypothesis that NPFWs cannot reach inner flowers, by measuring wasp and fig morphology at the species‐specific times of NPFW attack in the field. We found that three species of Sycoscapter and Philotrypesis wasps that parasitise pollinators could reach 34–73%, 75–92% and 82–97% of fig ovaries, respectively. Meanwhile, Eukobelea and Pseudidarnes gall‐formers, despite having shorter ovipositors, can access almost all fig flowers (93–99% and 100%), because they attack smaller (younger) fig fruits. Our mechanistic results from ovipositing wasps support spatial patterns of wasp offspring segregation within figs to suggest that inner ovules provide enemy‐free‐space for pollinators. This may contribute to mutualism stability by helping select for pollinators to avoid laying eggs where they are likely to be parasitised. These outer flowers then remain free to develop as seeds, promoting mutualism persistence.     

Relative investment in egg load and poison sac in fig wasps: Implications for physiological mechanisms underlying seed and wasp production in figs

Fig pollinating wasps and most non-pollinator wasps apply secretions from their poison sacs into oviposited flowers that appear necessary to the formation of the galls that their developing offspring consume. Thus, both eggs and poison sac secretions appear to be essential for wasp reproduction, but the relative investment in each is unknown. We measured relative investment in poison sac and egg production in pollinating and non-pollinating wasps associated with seven species of monoecious Panamanian figs representing both active and passive pollination syndromes. We then collected similar data for four fig hosts in China, where some wasp species in the genus Eupristina have lost the ability to pollinate (“cheaters”). All wasps examined possessed large poison sacs, and we found a strong positive correlation between poison sac size and absolute egg production. In the Panamanian species, the relative poison sac to egg investment was highest in the externally ovipositing non-pollinator wasps, followed by active pollinators, then by passive pollinators. Further, pollinator wasps of fig species with demonstrated host sanctions against “cheating” wasps showed higher investment in the poison sac than wasps of species without sanctions. In the Chinese samples, relative investment in the poison sac was indistinguishable between pollinators and “cheaters” associated with the same fig species. We suggest that higher relative investment in poison sac across fig wasp species reflects higher relative difficulty in initiating formation of galls and subsequently obtaining resources from the fig. We discuss the implications for the stability of the fig–wasp mutualism, and for the ability of non-pollinators to exploit this mutualism.     

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.     

Sexual differences in the attractiveness of figs to pollinators: females stay attractive for longer

1. Figs on male dioecious fig trees (Ficus, Moraceae) are breeding sites for pollinator fig wasps (Hymenoptera, Agaonidae), but figs on female plants are traps that produce only seeds. As the short‐lived fig wasps cannot reproduce in female figs, natural selection should favour individuals that avoid them. Several studies have failed to detect such discrimination, a result attributed to inter‐sexual mimicry and ‘selection to rush’ in the wasps, but their experiments failed to explicitly take into account fig age (how long they had been waiting to be pollinated). 2. We compared the relative attraction of male and female figs of known ages of the South East Asian Ficus montana Burm. f. to its pollina tor Liporrhopalum tentacularis Grandi and examined how the reproductive success of the plant and its pollinator change with the age of the figs. 3. Mean retention time for un‐pollinated figs on female plants was 16 days whereas in male figs it was 12 days. Female figs remained attractive for up to 2 weeks, although the wasps were less willing to enter older figs. After pollinator entry, receptivity continued for several days, lasting longer in figs entered by a single wasp. Consistent with abortion rates, attractiveness persisted longer in female figs. Older figs produced fewer fig wasp offspring, but similar numbers of seeds. 4. The sexual differences in floral longevity in F. montana may represent part of a previously un‐recognised reproductive strategy in some fig trees that allows male plants to ‘export’ pollinators while also maintaining a resident fig wasp population.     

Secondary galling: a novel feeding strategy among ‘non‐pollinating’ fig wasps from Ficus curtipes

相似文献   

Are nematodes costly to fig tree–fig wasp mutualists?

Most mutualisms are exploited by parasites, which must strike an evolutionary balance between virulence and long‐term persistence. Fig‐associated nematodes, living inside figs and dispersed by fig wasps, are thought to be exploiters of the fig–fig wasp mutualism. The life history of nematodes is synchronized with the fig development and adapted to particular developmental characteristics of figs. We expect host breeding systems (monoecious vs. gynodioecious figs) and seasonality to be central to this adaptation. However, the details of the adaptation are largely unknown. Here, we conducted the first field surveys on the prevalence of nematodes from monoecious Ficus microcarpa L.f. (Moraceae), gynodioecious Ficus hispida L.f., and their pollinating fig wasps in two seasons and two developmental stages of figs in Xishuangbanna, China. We followed this up by quantifying the effects of nematodes on fitness‐related traits on fig wasps (e.g., egg loads, pollen grains, and longevity) and fig trees (seed production) in gynodioecious F. hispida. The magnitude of nematode infection was compared between pre‐ and post‐dispersal pollinators to quantify the probability of nematodes being transported to new hosts. Our results showed that Ficophagus microcarpus (Nematoda: Aphelenchoididae) was the only nematode in F. microcarpa. In F. hispida, Martininema guangzhouensis (Nematoda: Aphelenchoididae) was the dominant nematode species, whereas Ficophagus centerae was rare. For both species of Ficus, rainy season and inter‐floral figs had higher rates of nematode infection than the dry‐hot season and receptive figs. Nematodes did not affect the number of pollen grains or egg loads of female wasps. We did not detect a correlation between seed production and nematode infection. However, carrying nematodes reduced the lifespan and dispersal ability of pollinator wasps, indicating higher rates of post‐emergence mortality in infected fig wasps. Severely infected fig wasps were likely ‘filtered out’, preventing the overexploitation of figs by wasps and stabilizing the interaction over evolutionary time.     

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.     

Competitive Exclusion among Fig Wasps Achieved via Entrainment of Host Plant Flowering Phenology

Molecular techniques are revealing increasing numbers of morphologically similar but co-existing cryptic species, challenging the niche theory. To understand the co-existence mechanism, we studied phenologies of morphologically similar species of fig wasps that pollinate the creeping fig (F. pumila) in eastern China. We compared phenologies of fig wasp emergence and host flowering at sites where one or both pollinators were present. At the site where both pollinators were present, we used sticky traps to capture the emerged fig wasps and identified species identity using mitochondrial DNA COI gene. We also genotyped F. pumila individuals of the three sites using polymorphic microsatellites to detect whether the host populations were differentiated. Male F. pumila produced two major crops annually, with figs receptive in spring and summer. A small partial third crop of receptive figs occurred in the autumn, but few of the second crop figs matured at that time. Hence, few pollinators were available to enter third crop figs and they mostly aborted, resulting in two generations of pollinating wasps each year, plus a partial third generation. Receptive figs were produced on male plants in spring and summer, timed to coincide with the release of short-lived adult pollinators from the same individual plants. Most plants were pollinated by a single species. Plants pollinated by Wiebesia sp. 1 released wasps earlier than those pollinated by Wiebesia sp. 3, with little overlap. Plants occupied by different pollinators were not spatially separated, nor genetically distinct. Our findings show that these differences created mismatches with the flight periods of the other Wiebesia species, largely ‘reserving’ individual plants for the resident pollinator species. This pre-emptive competitive displacement may prevent long term co-existence of the two pollinators.     

A comparison of pollinator fig wasp development in figs of Ficus montana and its hybrids with Ficus asperifolia

Figs (Moraceae) and pollinator fig wasps (Hymenoptera: Agaonidae) have a highly specific mutualistic relationship but fig wasps occasionally enter atypical hosts, and this can lead to hybrid fig trees and the potential for gene flow between species. Many fig trees are dioecious, with fig wasp offspring developing in galled ovules inside figs on male trees, whereas seeds develop only in figs on female trees. We generated experimental hybrids between the Asian Ficus montana Blume and a closely related African species Ficus asperifolia Miquel. Male F1s were sterile if entered by Kradibia tentacularis (Grandi) (Agaonidae), the pollinator of F. montana, because its offspring always failed to develop, without ovule enlargement. As with the F1s, figs on most male backcross plants [F. montana × (F. montana × F. asperifolia)] also aborted shortly after pollinator entry, resulting in a higher turnover of figs than with F. montana, although the times taken for the figs to reach receptivity were similar. Pollinator larvae nonetheless consistently managed to develop inside the figs of one backcross plant and also occasionally in a few figs from another backcross individual. In these figs, galled ovules developed as normal, whereas in figs that aborted the galled ovules failed to enlarge. The sex ratio of K. tentacularis progeny in the backcross figs was female biased and did not differ from that in F. montana figs. Sycoscapter spec. (Hymenoptera: Pteromalidae), a parasitoid of K. tentacularis, was able to lay eggs and developed normally inside male backcross figs where its host was present.     

Utilisation of chemical signals by inquiline wasps in entering their host figs

The fig tree, Ficus curtipes, hosts an obligate pollinating wasp, an undescribed Eupristina sp., but can also be pollinated by two inquiline (living in the burrow, nest, gall, or other habitation of another animal) wasps, Diaziella yangi and an undescribed Lipothymus sp. The two inquilines are unable to independently induce galls and depend on the galls induced by the obligate pollinator for reproduction and, therefore, normally enter receptive F. curtipes figs colonised by the obligate pollinators. However, sometimes the inquilines also enter figs that are not colonised by the pollinators, despite consequent reproductive failure. It is still unknown which signal(s) the inquilines use in entering the colonised and non-colonised figs. We conducted behavioural experiments to investigate several possible signals utilised by the inquilines in entering their host receptive figs. Our investigation showed that both inquiline species enter the receptive F. curtipes figs in response to the body odours of the obligate wasps and one of the main compounds emitted by the figs, 6-methyl-5-hepten-2-one. The compound was not found in the pollinator body odours, suggesting that the two inquiline wasps can utilise two signals to enter their host figs, which is significant for the evolution of the fig-fig wasp system. These inquilines could evolve to become mutualists of the figs if they evolve the ability to independently gall fig flowers; there is, however, another possibility that a monoecious Ficus species hosting such inquilines may evolve into a dioecious one if these inquilines cannot evolve the above-mentioned ability. Additionally, this finding provides evidence for the evolution of chemical communication between plants and insects.