Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): hypotheses for an ancient symbiosis

Figs and their pollinating fig wasps are dependent on one another for propagation of their own kinds. The wasps reproduce by ovipositing through the styles of female flowers within the closed fig receptacles (syconia). About half of the female flowers within the syconia of monoecious figs have styles which are longer than the ovipositors of the wasp, and they will therefore produce seeds rather than wasp larvae. Since a longer ovipositor would enable a wasp to reach more ovules and deposit more eggs, the question arises at to why longer ovipositors have not evolved.
In an attempt to answer this question, four seemingly plausible hypotheses are examined but each is shown to be problematical in some way. Consideration is then given to a fifth hypothesis which proposes that ovipositor length is constrained by abortion of syconia with relatively few seed embryos and many agaonid larvae. It is argued first that this pattern of abortion will be selected during a sustained period of heavy wasp infestation because seeds will then become scarce relative to pollen-carrying wasps. Increased expenditure by the fig on seed production would therefore be favoured by natural selection. A greater expenditure on seeds would occur if young syconia with exceptionally heavy wasp infestations were dropped and the saved nutrients invested in syconia of a subsequent crop containing average levels of wasp larvae and seeds. Provided that the energy and nutrient cost of dropping young syconia is small, the selective advantage to the wasp of longer ovipositors is eliminated in this way. A stable coexistence of figs and wasps is therefore possible. The paper concludes by discussing two general predictions of the abortion hypothesis, and how these may be tested.     

Development of 17 microsatellite markers for Ceratosolen constrictus, the pollinating fig wasp of Ficus fistulosa

The obligate mutualism between figs (Ficus) and fig pollinating wasps (Agaonidae) is regarded as a classic example of mutualism. Seventeen polymorphic microsatellite loci were developed for Ceratosolen constrictus, the pollinating wasp of the dioecious fig Ficus fistulosa. The number of alleles per locus ranged from two to 15 and the observed and expected heterozygosities ranged from 0.040 to 0.846 and from 0.040 to 0.916, respectively. These microsatellite loci offer a powerful tool for evolutionary and population genetic studies in C. constrictus, and gene flow of F. fistulosa.     

Rampant host switching and multiple female body colour transitions in Philotrypesis (Hymenoptera: Chalcidoidea: Agaonidae)

Figs (Ficus, Moraceae) and their associated fig waSPS (Hymenoptera, Chalcidoidea and Agaonidae) have attracted much attention and have been used as a model system for many studies. Fig waSPS belonging to the genus Philotrypesis are very common in most figs but their taxonomy, ecology and biology are currently poorly explored. A previous study on African Philotrypesis showed that their host association is phylogenetically conserved at subsection level. We reconstructed a molecular phylogeny with extended sampling from seven sections of figs. Our study suggested that the diversification of Philotrypesis is less constrained by host figs. Host switching is rampant between figs at species level and even at section level. We also investigated the evolution of the body colour forms in female Philotrypesis. Our study first suggested that female body colour is not evolutionarily stable and that there have been multiple transitions. Possible mechanisms for multiple colour transitions are expected to be determined in the near future.     

Substrate water potential constraints on germination of the strangler fig Ficus aurea (Moraceae)

Palms are the most common support hosts for strangler fig (Ficus aurea) in the tropical dry forest. At Hummingbird Cay Tropical Field Station in the Bahamas, viable F. aurea seeds scattered on open soil germinate within 6 d in the laboratory at 27C in light or darkness. To test the hypothesis that water relations between seed and substrate can restrict the site of F. aurea establishment, fig seeds were imbibed in mannitol solutions with water potential (psi) from 0 MPa to -2.0 MPa. At psi > -1.0 MPa, germination ranges from 70 to 90%. Below -1.0 MPa, germination drops under 4%. Seedling growth rate slows linearly with decreasing psi, due to reduced cell enlargement in the radicle. Sensitivity of F. aurea seeds to psi stress is similar to that of mesophytic crops with "threshold' psi of -1.2 to -1.5 MPa, below which germination and/or seedling growth stops. F. aurea shows no evidence of xerophytic adaptation in germination physiology. In the field, psi of humus in palm leaf bases does not drop below -1.0 to -1.1 MPa, while humus in terrestrial sites reaches psi F. aurea germination and seedling growth is met by humus in palm leaf bases, not by terrestrial sites. In dry forests, this restricts F. aurea establishment to the crown of palm trees.     

Disturbance effects on community structure of Ficus tinctoria fig wasps in Xishuangbanna, China: Implications for the fig/fig wasp mutualism

Abstract  Fig trees are important components of tropical forests, because their fruits are eaten by so many vertebrates, but they depend on pollinating fig wasps to produce mature fruits. Disturbance to habitat structure can have a major impact on insect diversity and composition, potentially reducing fruit yields. We investigated the impact of habitat disturbance on the fig wasp community associated with male figs of Ficus tinctoria in Xishuangbanna, China. The community comprised one pollinator species Liporrhopalum gibbosae and six non-pollinating wasp species: Sycoscapter sp.1, Philotrypesis ravii , Philotrypesis sp.1, Neosycophila omeomorpha , Sycophila sp.1, and Walkerella sp.1. More disturbed areas were characterized by higher temperatures, less shade, and more vehicle noise. The response of the fig wasp community was complex, with no simple relationship between intensity of disturbance and pollinator abundance. However, the sex ratios (proportion of male progeny) of pollinators increased significantly in more disturbed areas. We conclude that potential changes in fig wasp community composition brought about by disturbance, are unpredictable, with unclear consequences for tropical rainforest biodiversity.     

The Flight Heights of Chalcid Wasps (Hymenoptera,Chalcidoidea) in a Lowland Bornean Rain Forest: Fig Wasps are the High Fliers1

Tropical rain forests are characterized by their rich plant diversity and highly diverse insect faunas containing mainly rare species. Phytophagous and parasitoid insects utilizing such fragmented resources often must travel considerable distances to find suitable hosts. For small, weak‐flying insects, entry into the fast‐flowing air above the canopy can provide one way by which long‐distance dispersal is achieved. Using sticky traps placed at different heights in a lowland rain forest of Borneo, we compared the diurnal and nocturnal flight heights of chalcids, a group of mainly very small parasitoids and phytophages, to determine if the air above the canopy was used for dispersal. Most families were represented throughout the range of trap heights, including those above the general canopy. A higher proportion of individuals were trapped above the canopy at night than during the day. Fig wasps were exceptional in that they were trapped almost entirely above the canopy. They included species associated with host trees that do not fruit in the canopy, suggesting that these short‐lived, slow‐flying insects actively fly up above the canopy and then use the wind to passively carry them the long distances needed to reach their highly localized and ephemeral hosts. Once the fig wasps detect the species‐specific volatiles released by their host figs, they then may fly down into the canopy, where the lower wind speeds would allow them to fly actively upwind to their hosts.     

Schistonchus africanus n. sp. (Aphelenchida: Aphelenchoididae) Associated with Ficus thonningii (Moraceae) and its Pollinator Wasp Elisabethiella stuckenbergi (Chalcidoidea: Agaonidae)

Syconia ("figs") from Ficus thonningii and adults of its pollinator wasp Elisabethiella stuckenbergi were dissected to elucidate their association with a new species of Schistonchus (Aphelenchoididae). Schistonchus africanus n. sp. is characterized by a short stylet (13-16 μm long); position of the excretory pore opening in both sexes at a level just behind the stylet knobs; and short post-uterine branch, one body-width long. Schistonchus africanus n. sp. parasitizes F. thonningii florets and is transported by the winged females of E. stuckenbergi. Juveniles, females, and males of the nematode were found in the female and male fig florets and in the abdomen of the vector. Nematode populations extracted from female wasps or fig floret tissues did not differ in their morphology. No association was observed with the wingless males of the pollinator wasp.     

The role of animals in the colonization of the Krakatau Islands by fig trees (Ficus species)

Abstract. Since the biologically extirpating eruption of Krakatau (Sunda Strait) in 1883, Rakata (Krakatau's remnant) and two closely adjacent islands, Sertung and Panjang, have been colonized by over 200 species of vascular plants. They now carry species-poor mixed tropical forest, including some twenty-three species of Ficus . Data on the sequence of colonization over the last century by twenty-four Ficus species, twenty-three species of volant frugivores, and by agaonid fig-wasps, presumably from the large islands of Java and Sumatra, each some 44 km distant, are summarized. The potential of the volant frugivores as dispersers of fig seeds is assessed, the pollination problems involved in the colonization of islands by figs are reviewed and patterns of colonization by fig species and by their bird and bat dispersers are identified and discussed.
In 1930 a new island, Anak Krakatau, emerged from Krakatau's submerged caldera. This active volcano suffered a self-sterilizing eruption in 1952/1953 and has been colonized, under considerable constraint from its own volcanic activity, probably largely from the (selected) species pool present on Rakata, Sertung and Panjang, 2–4 km away. Its vegetation is at an earlier successional stage (grassland and Casuarina woodland) than that of the three older islands, and in 1992 the Casuarina woodland was in an early stage of transition to mixed forest. The colonization of Anak Krakatau by Ficus species, agaonid wasps and volant frugivores over a critical decade (1982–92) is reviewed, including preliminary assessments of the effects of pollinator limitation on four pioneer fig species and indications of a possible effect of the presence of avian raptors, particularly the peregrine falcon, on fig colonization and forest diversification.     

Isolation of six microsatellite loci in the pollinating fig wasp,Platyscapa awekei

Platyscapa awekei DNA was enriched for several repeat motifs. Sequencing of 48 transformed colonies showed that 22 contained microsatellite loci. Eleven of these loci were tested and six of them proved to be reliable and variable. As expected from these wasps’ biology, F_IS was high (= 0.423), indicating frequent sibmating. Notwithstanding, we estimate that dispersing males may secure as much as 8% of all matings.     

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

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

Maternal control of offspring sex and male morphology in the Otitesella fig wasps

Models concerning the evolution of alternative mating tactics commonly assume that individuals determine their own strategies. Here we develop a computer-based ESS model that allows mothers, ovipositing in discrete patches, to choose both the sex and the male mating tactics (natal-patch mating or dispersing) of their offspring based only on how many other mothers have used the specific patch before them. Data for three species of nonpollinating fig wasps from the Otitesella genus agree quantitatively with the model's assumptions and predictions. This suggests that females respond to population densities at the level of individual figs. The alternative male tactics in the species we studied are probably a result of a conditional strategy exercised by the mother that laid them. In addition, as females were only allowed to lay one egg per patch, our results suggest a new mechanism that can skew population sex ratios towards a female bias.     

雌花期榕小蜂进入榕果的行为及其活动时间

在西双版纳,钝叶榕传粉榕小蜂Eupristina sp.和杨氏榕树金小蜂Diaziella yangi均在雌花期进入钝叶榕果内繁殖和传粉,比较研究它们进入榕果的行为和活动时间。结果显示:在搜寻苞片处进蜂口时,2种榕小蜂的种内均出现打斗行为,并且杨氏榕树金小蜂的打斗更为激烈,但种间没有打斗行为发生,杨氏榕树金小蜂总是等待钝叶榕传粉榕小蜂先期进入榕果,然后才跟随着进入。在搜寻和进入苞片口通道阶段,钝叶榕传粉榕小蜂均比杨氏榕树金小蜂花费较长时间;而在果腔内产卵、传粉的时间,2种榕小蜂均最多不超过3d。相似的进蜂过程和活动时间,可能是2种榕小蜂与寄主榕树长期协同进化的结果。     

Characterization of microsatellite loci in the African fig Ficus sycomorus L. (Moraceae)

Microsatellite loci were characterized in the African fig tree Ficus sycomorus in order to investigate patterns of pollination and gene flow in this species. The loci characterized included new loci isolated from F. sycomorus and a single locus originally developed in Ficus carica. In total 12 loci were polymorphic when tested in between eight and 79 Namibian F. sycomorus individuals. Three of the new F. sycomorus loci were found to be polymorphic in cultivars of the edible fig F. carica suggesting a selection of these loci will be useful for population studies in other fig species.     

Isolation of microsatellite loci in the pollinating fig wasp of Ficus hispida, Ceratosolen solmsi

Microsatellite loci were isolated for Ceratosolen solmsi , pollinator of the dioecious Ficus hispida. We developed nine polymorphic microsatellite loci based on the method of polymerase chain reaction isolation of microsatellite arrays (PIMA). Enrichment of genomic libraries was performed by random amplified polymorphic DNA (RAPD). A subset of 38 positive clones was sequenced; 15 clones showed microsatellite loci. We tested 15 designed primer pairs and nine of them produced polymorphic amplification in 48 individual wasps collected from different fruits of the dioecious host fig Ficus hispida in China. Among the 48 individuals, 49 alleles were obtained at the nine loci. The observed heterozygosity ranged between 0.357 and 0.634.     

榕树传粉昆虫榕小蜂染色体制备方法研究

榕树与其传粉昆虫榕小蜂之间具有高度专一的互惠共生关系,榕小蜂为榕树传粉的同时又在榕果内营寄生生活,直至完成其整个生活史,因此一直以来对榕小蜂的染色体研究存在很大困难。本文以对叶榕Ficus hispida传粉榕小蜂Ceratosolen solmsi和鸡嗉子榕F.semicordata传粉榕小蜂C.gravelyi为材料,摸索出一套适合于榕树传粉昆虫榕小蜂染色体研究的详细、有效的技术和方法。应用该法对对叶榕传粉榕小蜂C.solmsi和鸡嗉子榕传粉榕小蜂C.gravelyi的染色体核型进行了研究,结果表明两种榕小蜂的染色体核型特征非常相似,具有相同的染色体数目2n(♀)=10,染色体类型全部为中着丝粒染色体,臂数NF=20。此外,在相对长度方面两者也没有明显的差异。最后与Imai等1988年研究蚂蚁染色体时提出的方法进行了比较。利用本文介绍的方法进行榕小蜂染色体制备,操作过程简单、重复性强,不仅能够得到大量的染色体分裂相,而且染色体细胞界限明确、形态清晰、分散良好。     

Effects of within-tree flowering asynchrony on the dynamics of seed and wasp production in an Australian fig species

Abstract. Within-tree flowering asynchrony in figs, which may allow pollinating wasps to avoid the risks of dispersal in inclement conditions, has been predicted as a trait to be favoured in highly seasonal environments. Comparisons of such asynchronous figs with better-known species that exhibit within-tree synchrony might also be expected to reveal differences in the outcome of the conflict between pollinator wasp and fig seed production, and the dynamics of non-pollinating wasps. This paper presents data on wasp and seed production in Ficus rubiginosa Desf. ex Vent., an asynchronous species that occurs in the highly seasonal environment of south-eastern Australia. In contrast to recent studies of figs showing within-tree flowering synchrony, syconium size was the main determinant of wasp and seed production in F. rubiginosa . Non-pollinating wasps were highly prevalent but occurred in low numbers and appeared to have relatively little impact on pollinator wasp or fig seed production. Data on flower positions revealed that non-pollinating wasps occurred almost exclusively in the outer layer of flowers, while pollinators were more abundant in the inner flower layer, which may represent an area of enemy-free space. The ratio of seeds to female pollinator wasps, an index of fig sex allocation, was more seed-biased than in several New World fig species that exhibit within-tree synchrony. This last result supports the idea that within-tree fruiting asynchrony permits a degree of self-pollination in F. rubiginosa .     

Cloning and immunolocalization of an antifungal chitinase in jelly fig (Ficus awkeotsang) achenes

A 30-kDa protein extracted from the pericarpial portion of jelly fig (Ficus awkeotsang Makino) achenes has been identified as a thermostable chitinase based on its enzymatic activity. A cDNA fragment encoding the precursor protein (including a cleavable signal sequence) of this chitinase was obtained by PCR cloning, and subsequently confirmed by immunological recognition of its overexpressed protein in Escherichia coli. Homology modeling predicted that this thermostable chitinase in jelly fig achenes comprised a stable (betaalpha)(8) barrel fold with three pairs of disulfide linkage. Immunostaining indicated that this chitinase was exclusively localized in the pericarpial region but not in the seed cells where bulky protein bodies and massive oil bodies were accumulated. Spore germination of Colletotrichum gloeosporioides, a common post-harvest pathogen infecting ripening fruit of jelly fig and many other fruits, was inhibited by this chitinase purified from achenes. It is suggested that the biological function of the thermostable chitinase in the pericarp of jelly fig achenes is to protect the nutritive seeds from fungal attack during fruit ripening.     

Independent evolution of the same set of characters in fig flies (Lissocephala,Drosophilidae)

Summary Comparison of species of African fig flies (Lissocephala, Drosophilidae) shows that an unusual phenotype has evolved independently when a particular environment prevails. Each time the adaptation is observed, associated morphological and behavioural characters also appear. Such convergence suggests that selection operates on sets of predetermined morphogenetic pathways.