Shift To Mutualism In Parasitic Lineages Of The Fig-wasp Interaction

The interaction between fig trees (Ficus) and their pollinating fig wasps (Agaonidae) represents a remarkable example of mutualism and coevolution, each needing the other for reproduction. In addition of pollinating fig wasp species, figs host a suite of parasites of the mutualism belonging to other chalcidoid families. As with the agaonids, these fig wasps develop in fig flowers, but do not usually pollinate their hosts, hence they are commonly called non-pollinating fig wasps (NPFW). Most non-agaonid wasps oviposit through the fig wall from outside the fig. A small number of non-agaonid fig wasps (subfamilies Sycoecinae. Sycophaginae and Otitesellinae) are exceptional in that, like agaonids. These non-pollinating fig wasp species do not belong in the agaonid lineage. They have foundresses that enter the figs and oviposit in the female flowers, just as agaonid wasps do. Here, we report occurrence of internally ovipositing wasps in genus Eupristina poliinated fig species. And we conduct experimental introductions in order to study the reproductive ecology and the relationships between the host figs (Ficus curtipes and Ficus glaberrima), their regular agaonid pollinators Eupristina spp.. and the internally oviposting non-agaonid wasps( Diaziella yangi, Diaziella bizarrea and Lipothymus sp.). Furthermore, the mechanism of the evolution from parasite to mutualism in parasitic lineages of the fig-wasp interaction is studied. These results are very useful for understanding the origin of the fig-fig wasp mutualism. The main results are as follows.1. Two species of figs (Ficus curtipes and Ficus glaberrima) that are pollinated by genus Eupristina also host specific fig wasps belonging to the chalcidoid genera Diaziella (S ycoecinae) and Lipothymus (Otitesellinae) among ten species of figs observed. F. curtipes is passively pollinated. Other eight Ficus species (Ficus glaberrrima, F. altissima, F. benjamina, F. stricta, F. microcarpa, F. macellandi, Ficus sp. and F. drupacea pubescens) are actively pollinated. The anther-to-ovule ratio of F. hookeriana is high (0.56), but its corresponding pollinating fig wasps have well defined thoracic pollen pockets (to carry pollen) and coxal combs on their fore coxae (to manipulate pollen). So pollination mode of F. hookeriana is not confirmed now. Internally ovipositing non-agaonids occur both in passively and actively pollinated Ficus species.2. Internally ovipositing non-agaonids and pollinating fig wasps enter figs and oviposit in the same time (female flower phase). Their females do actively seek out figs entered by Eupristina spp.. Internally oviposting non-agaonids Diaziella yangi and Lipothymus sp. can pollinate in passively pollinated F. curtipes. As the number of conspecific foundresses per fruit increased, the number of seeds produced increased. Sometimes the pollination efficiency of D. yangi and Lipolhymus sp. was even higher than that of Eupristina sp.. D. bizarrea can not be a similarly effective pollinator of Ficus glaberrima. an actively pollinated monoecious fig tree. Internally ovipositing non-agaonids failed to reproduce independently in passively or actively pollinated Ficus species, they depend on the agaonid, Eupristina, to make galls. Both species of fig-entering non-agaonid wasps significantly reduced the number of regular pollinators emerging from mature figs but had no effect on seed production. Internally ovipositing non-agaonid fig wasps have built the mutualism with their hosts, but they can not replace the regular pollinating fig wasps. As far as these internally ovipositing non-agaonid fig wasps can make galls, they can constitute the species-specific mutualism.3. The mating mode of internally non-agaonids was not identical to the results thoroughly predicted by wing morphs of males. Although they are winged, most of Diaziella yangi and D. bizarrea mated inside the figs in which they developed, and males had intensely fighting behavior for mating opportunities. On the contrary, although Lipothymus sp. was wingless, part of mates occurred outside the figs. These internally ovipositing non-agaonids followed the partial local mate competition. All the mates of regular pollinators with wingless males occurred inside the figs in which they developed, which followed LMC (Local Mate Competition). This showed that it was inaccurate to predict the mating mode only according to male morphs. The average sex ratio of the pollinator(Eupristina sp.) of F. curtipes was significantly higher than the average sex raio of D. yangi. However, there was no significantly difference between the average sex ratio of Eupristina sp. and Lipothymus sp, and there was no also significantly difference between the average sex ratio of D. yangi and Lipothymus sp. The average sex ratio of the pollinator (Eupristina sp.) of F. glaberrima was significantly higher than the average sex ratio of D. bizarrea. And there were not significant positive correlations between the averge sex ratio of three internally ovipositing non-agaonids (D. yangi, D. bizarrea and Lipothymus sp.) and the proportion of fruit in which it occurred.4. Figs of the monoecious fig trees Ficus curtipes and F. glaberrima (subsection Conosycea) lack a synstigma. which is replaced by an irregular mass of elongate stigmas. The pollinators of F. curtipes and F. glaberrima do not oviposit via the top of the stigmas, but insert their ovipositors through the stigmal bases. Oviposition behavior in fig wasps is therefore responsive to variation in floral structure within their host figs.5. Eupristina sp. progeny was not correlated with seeds in the three years (2006.2007 and 2008). The number of Eupristina sp. progeny per fig during the colder month (December 2006) was significantly higher than during the wanner month (August 2007; July 2008) (LSD:P< 0.05). There was no significant difference in the number of Diaziella bizarrea progeny during three years. D. bizarrea. Sycoscapier sp.. and Philotrypesis sp. occurred consistently.as the most common fig wasps every year. This result suggested that some fig wasps showed a certain degree of season recurrence or specificity, and the composition of fig wasps was not conspicuously influenced by the seasonal factor.6. Compared with the fig trees reported, the two partners in Ficus curiipes and F. glaberrima were also highly co-adapted in many aspects, for example, phenology, between the pollination behavior and A/O ratio, etc. In Ficus curtipes, in addition to regular pollinating fig wasp, it hosts two internally oviopositing non-agaonid fig wasps, they can pollinate for F. curtipes. F. curtipes and F. glaberrima often produced more same-phase syconia within one tree.7. For Ficus curtipes and F. glaberrima, non-pollinating fig wasps allocate resources through differentiation in oviposition time and larval diet. The non-pollinating fig wasps had significantly negative effects on pollinating fig wasps, but there were no correlations between the number of pollinating fig wasps and the number of seeds.8. At post-floral phase of syconia of Ficus glaberrima, wasp offspring and galler near the cavity were larger; wasp offspring and galler near the wall were smaller. Seeds near the wall were larger, and germination rate were higher and faster, while seeds near the cavity were smaller, and germination rate were lower and slower. Wasps prefer to oviposit in the female flowers near fig cavity to benefit the development of offspring. While female flowers near the wall were more likely to receive pollens to benefit the development and germination of seeds.