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.     

聚果榕传粉榕小蜂传粉与产卵之间的权衡

【目的】榕树(Ficus)依赖专性榕小蜂(Agaonidae)传粉,同时为传粉榕小蜂提供繁衍后代的场所,两者形成动植物间经典的协同进化关系。在雌花期果内,榕小蜂需在有限的存活时间内完成传粉和产卵,而传粉榕小蜂如何在传粉与产卵之间进行权衡仍然是悬而未解的问题。本研究旨在明确传粉榕小蜂——一种栉颚榕小蜂Ceratosolen sp.在雌雄同株的聚果榕Ficus racemosa雌花期果内的行为活动及繁殖模式。【方法】借助测微尺测量聚果榕榕果雌花花柱长度与传粉榕小蜂(Ceratosolen sp.)产卵器长度,通过显微视频记录传粉榕小蜂在雌花期果内搜索、传粉及产卵行为;结合单果控制性引蜂试验,测定不同阶段榕小蜂个体大小、孕卵量、携粉量,以及雄花期最终繁殖的榕小蜂后代和榕果种子数量。【结果】聚果榕雌花花柱长度存在树间变异,榕小蜂产卵器长度比绝大多数的雌花花柱长,说明该小蜂可以产卵于大部分的雌花子房里。通常个体大的榕小蜂孕卵量更多,但个体大小与携粉量之间相关性不显著。观察发现,榕小蜂进入雌花期榕果内,前6 h集中产卵,可产下孕卵量的95%,平均搜索用时27 s,产卵用时46 s,此期间传粉行为少见,花粉筐中携带花粉量亦无明显变化;榕小蜂进果后6-24 h,主要执行传粉,其行为主动,连贯高效,单次传粉用时平均为2 s,最终可传完携粉量的80%。控制引蜂试验也证实榕小蜂进入榕果内前6 h主要执行产卵繁殖后代,之后6-24 h主要执行传粉以繁殖榕树种子。【结论】在雌雄同株的聚果榕雌花期榕果内,榕小蜂先产卵、后传粉。本研究首次展示了传粉榕小蜂在聚果榕雌花期榕果内的产卵和传粉行为,并获得与行为相匹配的产卵量和传粉繁殖量,反映了具主动传粉行为的榕小蜂在传粉和产卵之间存在时间和数量上的权衡。     

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.     

Plasticity and diversity of the phenology of dioecious Ficus species in Taiwan

While Ficus present a series of traits often associated with dioecy, the prevalence of dioecy in Ficus is atypical. In Asian floras, dioecious Ficus species generally outnumber monoecious ones. Further this is also true in relatively northerly locations for Ficus such as the island of Taiwan. Ficus are pollinated by species-specific wasps that use fig flowers as breeding sites. In dioecious fig species, pollinators develop only in the inflorescences of male fig trees. In this study, we investigated the reproductive phenology of four dioecious Ficus species with distinct ecologies in several locations in northern and southern Taiwan. The two first species (Ficus erecta and Ficus septica) were investigated in four locations. Reproductive phenology was quite different among sites, even within a single species. For example, F. erecta presented well-defined crops at the population level in its usual high-elevation habitat but continuous fig production at low elevations, especially in South Taiwan. The two other fig species (Ficus pedunculosa var. mearnsii and Ficus tinctoria subsp. swinhoei), are shrubs growing together along seashores in exposed locations on coral reef remnants. These two species presented quite different traits allowing the survival of pollinating wasp populations. Ficus pedunculosa var. mearnsii produced figs continuously so that fresh receptive figs were always available for the pollinating wasps while F. tinctoria subsp. swinhoei extended the period of receptivity of its figs, so that receptive figs that had been waiting for pollinating wasps were almost always available. In summary, dioecious figs in Taiwan showed remarkable variation in their phenology, within species among locations or among species within location. Nevertheless, despite this variation, the phenology of the trees always allowed survival of pollinating wasp populations. Dioecious figs seem to have adopted a differentiated set of strategies which result in high resilience of pollinator populations. This resilience could help explain the atypical prevalence of dioecy in Ficus.     

Phenological Adaptations in Ficus tikoua Exhibit Convergence with Unrelated Extra-Tropical Fig Trees

Flowering phenology is central to the ecology and evolution of most flowering plants. In highly-specific nursery pollination systems, such as that involving fig trees (Ficus species) and fig wasps (Agaonidae), any mismatch in timing has serious consequences because the plants must balance seed production with maintenance of their pollinator populations. Most fig trees are found in tropical or subtropical habitats, but the dioecious Chinese Ficus tikoua has a more northerly distribution. We monitored how its fruiting phenology has adapted in response to a highly seasonal environment. Male trees (where fig wasps reproduce) had one to three crops annually, whereas many seed-producing female trees produced only one fig crop. The timing of release of Ceratosolen fig wasps from male figs in late May and June was synchronized with the presence of receptive figs on female trees, at a time when there were few receptive figs on male trees, thereby ensuring seed set while allowing remnant pollinator populations to persist. F. tikoua phenology has converged with those of other (unrelated) northern Ficus species, but there are differences. Unlike F. carica in Europe, all F. tikoua male figs contain male flowers, and unlike F. pumila in China, but like F. carica, it is the second annual generation of adult wasps that pollinate female figs. The phenologies of all three temperate fig trees generate annual bottlenecks in the size of pollinator populations and for female F. tikoua also a shortage of fig wasps that results in many figs failing to be pollinated.     

Age at pollination modifies relative male and female reproductive success in a monoecious fig tree

Plants that depend on a single species of insect pollinator must often contend with infrequent and unpredictable visitation. Prolongation of floral receptivity comes at the cost of reduced male and/or female reproductive success among older flowers. Fig trees (Ficus spp.) have a highly specific pollination symbiosis and individual inflorescences (syconia) that remain receptive for days or weeks. Reproductive success in monoecious fig trees involves production of both seeds and fig wasp offspring. We assessed whether the reproductive output of individual syconia changes with the length of time they waited for pollination, and whether the relative female and male reproductive success also changes. A pollination experiment was conducted in an SE Asian monoecious fig tree Ficus curtipes, in which receptive syconia were covered with mesh bags to exclude wasps and pollinated by single pollinators of this fig tree at their different receptive ages. When the syconia matured their size and contents were recorded. Seed quality was also assessed. The results showed that pollinators entered syconia that had been waiting for up to 36?days. The frequencies of abortions among syconia pollinated at different ages were low throughout. The number of un-utilised flowers increased progressively in older syconia. Seed production was highest in syconia entered on the first day of receptivity, whereas pollinator production peaked in syconia pollinated on day 12, then declined in older syconia. Consequently, overall reproductive efficiency declined with syconium age and floral sex allocation became more male-biased in older syconia. Older syconia also produced lighter seeds. These results suggest that un-pollinated syconia of F. curtipes can remain receptive for several weeks. This makes pollination of each syconium more likely, but at the cost of reduced productivity and with more ovules allocated to male function. However, the prolongation of floral receptivity has significance for the co-adaptation between syconia and fig wasps and for the evolution of the fig tree-fig wasp symbiosis.     

鸡嗉子榕隐头果雌花期特征对传粉榕小蜂选择的影响

为了探讨榕树隐头果的发育期、性别、大小等外部特征对传粉榕小蜂选择的影响,采取人为控制雌花期的方法,对鸡嗉子榕(Ficus sermicordata)及其传粉榕小蜂(Ceratosolen gravelyi)的选择行为进行研究。结果表明,在隐头花序发育到雌花期后,如果阻止传粉小蜂进入,隐头果会继续生长。直径较小的雌果和雄果的进蜂量较多,且在雌雄果同时存在时,小蜂仍然会选择进入雌果,但进蜂量显著低于雄果。小蜂优先选择进入雌花期前期的隐头花序,雌雄果皆有此特点。对于相同发育期的隐头果,果径和进蜂量呈正相关关系,说明对于相同发育期的隐头果,小蜂更倾向于进入较大的隐头果。因此,真正控制小蜂行为的是隐头花序所处的发育期,以及不同发育期所产生的化学挥发物,而非隐头果直径大小。这为进一步研究榕-蜂系统的稳定机制提供依据。     

Extremely high proportions of male flowers and geographic variation in floral ratios within male figs of Ficus tikoua despite pollinators displaying active pollen collection

Most plants are pollinated passively, but active pollination has evolved among insects that depend on ovule fertilization for larval development. Anther‐to‐ovule ratios (A/O ratios, a coarse indicator of pollen‐to‐ovule ratios) are strong indicators of pollination mode in fig trees and are consistent within most species. However, unusually high values and high variation of A/O ratios (0.096–10.0) were detected among male plants from 41 natural populations of Ficus tikoua in China. Higher proportions of male (staminate) flowers were associated with a change in their distribution within the figs, from circum‐ostiolar to scattered. Plants bearing figs with ostiolar or scattered male flowers were geographically separated, with scattered male flowers found mainly on the Yungui Plateau in the southwest of our sample area. The A/O ratios of most F. tikoua figs were indicative of passive pollination, but its Ceratosolen fig wasp pollinator actively loads pollen into its pollen pockets. Additional pollen was also carried on their body surface and pollinators emerging from scattered‐flower figs had more surface pollen. Large amounts of pollen grains on the insects' body surface are usually indicative of a passive pollinator. This is the first recorded case of an actively pollinated Ficus species producing large amounts of pollen. Overall high A/O ratios, particularly in some populations, in combination with actively pollinating pollinators, may reflect a response by the plant to insufficient quantities of pollen transported in the wasps’ pollen pockets, together with geographic variation in this pollen limitation. This suggests an unstable scenario that could lead to eventual loss of wasp active pollination behavior.     

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.     

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.     

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.     

THE STABILITY OF THE SYMBIOSIS BETWEEN DIOECIOUS FIGS AND THEIR POLLINATORS: A STUDY OF FICUS CARICA L. AND BLASTOPHAGA PSENES L.

Each Ficus species depends on a specific mutualistic wasp for pollination. The wasp breeds on the fig, each larva destroying a female flower. It is, however, not known why the wasps have not evolved the ability to use all female flowers. In “dioecious” figs, the wasp can only breed in the female flowers of the “male” trees, so that pollination of a female tree is always lethal. The wasps should therefore be selected to avoid female trees. Field data is presented showing that the fruiting phenology of the dioecious fig Ficus carica is such that this selection does not occur: syconia are not receptive at the same time on “male” and female trees. Most wasps are forced to emerge from the syconia of “male” trees at a time when they will not be able to reproduce, whether they avoid female trees or not. This aspect of the life cycle of the wasp, although noticed, has been obscured in most previous studies. It is shown that the fruiting phenology of Ficus carica, which stabilizes the symbiosis, is the result of short-term selective pressures on the male function of the trees. Such selective pressures suggest a possible pathway from monoecy to dioecy in Ficus under seasonal climates.     

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.     

Can fine-scale post-pollination variation of fig volatile compounds explain some steps of the temporal succession of fig wasps associated with Ficus racemosa?

Volatile organic compounds (VOCs) emitted by flowers play an essential role in mediating the attraction of pollinators. However, they also attract other species exploiting resources associated with flowers. For instance, VOCs emitted by figs play a major role in encounters between Ficus spp., their mutualistic pollinating wasps, and all the members of the community of non-pollinating fig wasps (NPFWs) that exploit the mutualistic interaction. Because pollinators might be in limited supply for a tree bearing many inflorescences, the plant might maximize its individual reproductive success by reducing the attractiveness of inflorescences once they are pollinated, so that pollinators orient only towards the tree's unpollinated figs. Changes in VOCs emission that bring this about could represent an important cue for NPFWs that exploit particular stages of fig development. In this study, by monitoring precisely the presence of fig-associated wasps on figs of F. racemosa, a common widespread fig species, we demonstrated that 4–5 days and 15 days following pollination represent two critical transitional steps in the succession of different wasp species. Then, focusing on the first one of these transitional steps, by investigating the composition of fig VOCs at receptivity and from 1 to 5 days following pollination, we detected progressive quantitative and qualitative variation of floral scent following pollination. These changes are significant at 5 days following pollination. The qualitative changes are mainly due to an increase in the relative proportions of two monoterpenes (α-pinene and limonene). These variations of the floral VOCs following pollination could explain why pollinating wasps stop visiting figs very shortly after the first pollinators enter receptive figs. They also possibly explain the succession of non-pollinating wasps on the figs following pollination.     

A comparison of growth and reproduction, under laboratory conditions, of males and females of a dioecious fig tree

The interaction between Ficus spp. (Moraceae) and their pollinating wasps (Chalcidoidae: Agaonidae) is a highly co-evolved mutualism. Approximately half of all fig species are monoecious and produce a mixture of wasps and seeds within the same fig. In functionally dioecious fig trees male and female functions are separate. Figs on male trees produce wasps and pollen, whereas figs borne on female plants produce only seeds. Dioecious fig phenology provides an excellent opportunity to investigate the effect of sexual specialization on the obligate fig?Cfig wasp interaction and the non-pollinators associated with the system. Here we describe laboratory studies of phenological variation between two sexes in terms of vegetative growth and fig production in a dioecious fig tree Ficus montana. We also describe reproductive output in terms of wasp production in males and seeds in females. Intrasexual asynchrony was observed for the plants, with synchrony between the sexes with year-round production of figs. Male plants grew more rapidly, but leaf phenology was very similar. Crop sizes and development times were the same for males and females. Seasonal effects were strong for leaf phenology and fig initiation, but had a very limited effect on fig composition. The results show that the phenological differences described for other dioecious figs do not apply to all species.     

Chemosensory attraction of fig wasps to substances produced by receptive figs

In the mutualism between figs (Ficus spp., Moraceae) and their species-specific fig wasp pollinators (Hymenoptera: Agaonidae), location of a receptive host tree by the adult insect is a critical step. The adult female wasp lives only a few days, and must usually fly to a different tree than her natal tree to locate receptive figs. Trees in receptive phase often occur at very low densities. Reproductive success of both fig and wasp depends on trasmission of a very strong signal by the plant. Some evidence exists for the role of olfaction in location of receptive hosts by fig wasps, but very little work has been done on the chemical ecology of host location and host specificity. Here the first experimental evidence is presented for long-distance olfactory attraction of wasps by volatile substances produced by receptive figs, and for short-distance or contact chemostimulation by host volatiles that elicit entry of the wasp into the fig. In studies usingFicus carica L., pentane extracts of receptive-phase figs attract the pollinatorBlastophaga psenes L. from distances of at least 5 m in the field. Short-distance chemostimulation was demonstrated in laboratory bioassays. Pentane extracts of receptive figs, when painted onto the ostiole of non-receptive figs, elicit entry of pollinator wasps. Figs emit volatile compounds attractive to pollinating wasps only during the period of receptivity; pentane extracts of non-receptive figs are not attractive. A simple reliable procedure is described to compare the attractivity of different types of extracts (total, internal, and external extracts) and of different fractions, in the first step towards identifying attractant substances.     

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.     

Foundress Fig Wasps are More Likely to Re-emerge From Older Figs

The mutualistic interaction between Ficus spp. and their pollinating fig wasps (Agaonidae) centres on the plants’ unique inflorescences—their figs. Each Ficus species is pollinated by foundresses of host-specific fig wasps which enter figs to lay eggs in the female flowers. Most foundresses are trapped in the first figs they enter, but in some species wingless foundresses can re-emerge and subsequently enter and oviposit into further figs. We investigated whether number of potential oviposition sites, age of the fig and age of the wasp influence the likelihood of re-emergence of lone foundresses of the Asian fig wasp Kradibia (=Liporrhopalum) tentacularis from previously un-entered figs of Ficus montana. Likelihood of re-emergence was not influenced by wasp age or flower numbers (resource abundance), but was more frequent from older figs that had waited longer to be pollinated. Laying eggs in several figs offers clear advantages, but foundresses often failed to re-emerge despite being unable to lay all their eggs. Resource quality not quantity appears to be the main influence on the fig wasp’s oviposition decisions. The physical difficulty that the wasps experience when trying to re-emerge may prevent it, even when re-emergence would be advantageous for both the insect and its host plant, but older fig wasps were not detectably ‘weaker’ than younger individuals.     

Finding hidden females in a crowd: Mate recognition in fig wasps

Multi-species mating aggregations are crowded environments within which mate recognition must occur. Mating aggregations of fig wasps can consist of thousands of individuals of many species that attain sexual maturity simultaneously and mate in the same microenvironment, i.e, in syntopy, within the close confines of an enclosed globular inflorescence called a syconium – a system that has many signalling constraints such as darkness and crowding. All wasps develop within individual galled flowers. Since mating mostly occurs when females are still confined within their galls, male wasps have the additional burden of detecting conspecific females that are “hidden” behind barriers consisting of gall walls. In Ficus racemosa, we investigated signals used by pollinating fig wasp males to differentiate conspecific females from females of other syntopic fig wasp species. Male Ceratosolen fusciceps could detect conspecific females using cues from galls containing females, empty galls, as well as cues from gall volatiles and gall surface hydrocarbons.In many figs, syconia are pollinated by single foundress wasps, leading to high levels of wasp inbreeding due to sibmating. In F. racemosa, as most syconia contain many foundresses, we expected male pollinators to prefer non-sib females to female siblings to reduce inbreeding. We used galls containing females from non-natal figs as a proxy for non-sibs and those from natal figs as a proxy for sibling females. We found that males preferred galls of female pollinators from natal figs. However, males were undecided when given a choice between galls containing non-pollinator females from natal syconia and pollinator females from non-natal syconia, suggesting olfactory imprinting by the natal syconial environment.     

The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.