The evolution of parasitism from mutualism in wasps pollinating the fig, Ficus microcarpa, in Yunnan Province, China.

Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory's relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a "cheater" that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.

Defence mechanisms of Ficus: pyramiding strategies to cope with pests and pathogens.

Ficus species have adapted to diverse environments and pests by developing physical or chemical protection strategies. Physical defences are based on the accumulation of minerals such as calcium oxalate crystals, amorphous calcium carbonates and silica that lead to tougher plants. Additional cellular structures such as non-glandular trichomes or laticifer cells make the leaves rougher or sticky upon injury. Ficus have also established structures that are able to produce specialized metabolites (alkaloids, terpenoids, and phenolics) or proteins (proteases, protease inhibitors, oxidases, and chitinases) that are toxic to predators. All these defence mechanisms are distributed throughout the plant and can differ depending on the genotype, the stage of development or the environment. In this review, we present an overview of these strategies and discuss how these complementary mechanisms enable effective and flexible adaptation to numerous hostile environments.

Bioactive compounds content and their biological properties of acetone extract of Cuscuta reflexa Roxb. grown on various host plants.

The present study is aimed to evaluate the total phenolic and flavonoid contents, and free phenolic compounds of acetone extract of Cuscuta reflexa grown on five different hosts: Coccinia grandis, Ficus racemosa, Samanea saman, Streblus asper and Zollingeria dongnaiensis, and to explore the antioxidant activities, α-glucosidase and tyrosinase inhibitory properties of the extracts. The highest level of total phenolic and flavonoid contents were observed in the extract of C. reflexa that was grown on S. asper (65.45 mg GAE/g extract) and C. grandis (97.83 mg QE/g extract), respectively. According to HPLC results, vanillic acid, rutin and quercetin were found in all extracts of C. reflexa grown on diversified hosts. The extract of C. reflexa grown on C. grandis possessed the greatest antioxidant activities (DPPH; 251.64 µg/mL, FRAP; 26.44 mg GAE/g extract), α-glucosidase inhibition accounted for 84.36 per cent and antityrosinase activity was at 18.29 mg KAE/g sample.

The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues.

BACKGROUND AND AIMS: Pollinator specificity facilitates reproductive isolation among plants, and mechanisms that generate specificity influence species boundaries. Long-range volatile attractants, in combination with morphological co-adaptations, are generally regarded as being responsible for maintaining extreme host specificity among the fig wasps that pollinate fig trees, but increasing evidence for breakdowns in specificity is accumulating. The basis of host specificity was examined among two host-specific Ceratosolen fig wasps that pollinate two sympatric varieties of Ficus semicordata, together with the consequences for the plants when pollinators entered the alternative host variety. METHODS: The compositions of floral scents from receptive figs of the two varieties and responses of their pollinators to these volatiles were compared. The behaviour of the wasps once on the surface of the figs was also recorded, together with the reproductive success of figs entered by the two Ceratosolen species. KEY RESULTS: The receptive-phase floral scents of the two varieties had different chemical compositions, but only one Ceratosolen species displayed a preference between them in Y-tube trials. Specificity was reinforced at a later stage, once pollinators were walking on the figs, because both species preferred to enter figs of their normal hosts. Both pollinators could enter figs of both varieties and pollinate them, but figs with extra-varietal pollen were more likely to abort and contained fewer seeds. Hybrid seeds germinated at normal rates. CONCLUSIONS: Contact cues on the surface of figs have been largely ignored in previous studies of fig wasp host preferences, but together with floral scents they maintain host specificity among the pollinators of sympatric F. semicordata varieties. When pollinators enter atypical hosts, post-zygotic factors reduce but do not prevent the production of hybrid offspring, suggesting there may be gene flow between these varieties.

Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism.

Theory predicts that mutualisms should be vulnerable to invasion by cheaters, yet mutualistic interactions are both ancient and diverse. What prevents one partner from reaping the benefits of the interaction without paying the costs? Using field experiments and observations, we examined factors affecting mutualism stability in six fig tree-fig wasp species pairs. We experimentally compared the fitness of wasps that did or did not perform their most basic mutualistic service, pollination. We found host sanctions that reduced the fitness of non-pollinating wasps in all derived, actively pollinated fig species (where wasps expend time and energy pollinating), but not in the basal, passively pollinated fig species (where wasps do not). We further screened natural populations of pollinators for wasp individuals that did not carry pollen ('cheaters'). Pollen-free wasps occurred only in actively pollinating wasp species, and their prevalence was negatively correlated with the sanction strength of their host species. Combined with previous studies, our findings suggest that (i) mutualisms can show coevolutionary dynamics analogous to those of 'arms races' in overtly antagonistic interactions; (ii) sanctions are critical for long-term mutualism stability when providing benefits to a host is costly, and (iii) there are general principles that help maintain cooperation both within and among species.

Host pollination mode and mutualist pollinator presence: net effect of internally ovipositing parasite in the fig-wasp mutualism.

The Ficus-their specific pollinating fig wasps (Chalcidoidea, Agaonidae) interaction presents a striking example of mutualism. Figs also shelter numerous non-pollinating fig wasps (NPFW) that exploit the fig-pollinator mutualism. Only a few NPFW species can enter figs to oviposit, they do not belong to the pollinating lineage Agaonidae. The internally ovipositing non-agaonid fig wasps can efficiently pollinate the Ficus species that were passively pollinated. However, there is no study to focus on the net effect of these internally ovipositing non-agaonid wasps in actively pollinated Ficus species. By collecting the data of fig wasp community and conducting controlled experiments, our results showed that internally ovipositing Diaziella bizarrea cannot effectively pollinate Ficus glaberrima, an actively pollinated monoecious fig tree. Furthermore, D. bizarrea failed to reproduce if they were introduced into figs without Eupristina sp., the regular pollinator, as all the figs aborted. Furthermore, although D. bizarrea had no effect on seed production in shared figs, it significantly reduced the number of Eupristina sp. progeny emerging from them. Thus, our experimental evidence shows that reproduction in Diaziella depends on the presence of agaonid pollinators, and whether internally ovipositing parasites can act as pollinators depends on the host fig's pollination mode (active or passive). Overall, this study and others suggest a relatively limited mutualistic role for internally ovipositing fig wasps from non-pollinator (non-Agaonidae) lineages.

Pollen waste and unrelated traits in a fig-fig wasp symbiosis: a new behaviour suggesting a host shift.

In a fig-fig wasp symbiosis, we have discovered that male fig pollinators (Alfonsiella fimbriata Waterston) bite into the dehiscent anthers of Ficus natalensis leprieuri Miq., thus scattering the pollen grains throughout the syconium. Female pollinators are the only ones to transfer pollen to conspecific trees, and collect pollen actively from the anthers only. Thus, this male behaviour appears to be antagonistic to the pollination process. We compare different wasp pollinating behaviours between fig species exhibiting dehiscent and non-dehiscent anthers and conclude that this male behaviour is new and not required with spontaneously dehiscent anthers. These findings could suggest a host shift of Alfonsiella fimbriata.

[Comparison of habitats and seasonally differentiated distribution patterns of fig wasp populations associated with Ficus racemosa in Xishuangbanna].

The population distribution patterns of fig wasps associated with Ficus racemosa in Xishuangbanna were studied by using several indexes. The results indicated that the distribution patterns of 6 fig wasp species were all clump. The aggregative intensity of pollinating wasp (Ceratosolen fusciceps) population at primeval rain forest was nearly equal to that at seriously disturbed site, whereas they were both much higher than that at moderately disturbed site. In the meanwhile, the population aggregative intensity for the same wasp species was higher in rainy season than in dry-hot season, and the lowest was occurred in foggy-cool season. Non-pollinating wasp (Platyneura testacea, Platyneura mayri, Platyneura agraensis, Apocrypta westwoodi, Apocrypta sp.) population and each of their sex group were varied significantly in aggregative intensity, responding to the habitat change and seasonal alteration. The protection of original habitat should be focused on the protection of the mutualism of Ficus racemosa and fig wasps.

Fig wasp dispersal and the stability of a keystone plant resource in Borneo.

The stability of interactions in remaining rainforest fragments is an issue of considerable concern for conservation. Figs are a pre-eminent tropical keystone resource because of their importance for wildlife, but are dependent on tiny (1-2 mm) species-specific wasps for pollination. To investigate fig wasp dispersal I trapped insects at various heights (5-75 m) in an isolated fragment (ca. 4500 ha) of Bornean rain forest. Fig wasps constituted the majority of captures above the canopy (pollinators 47%, non-pollinators 5%). However, genera were not evenly represented. There were 50% more species of monoecious fig pollinator than there were host species in the fragment, indicating some must have arrived from forests with different assemblages of figs at least 30 km away. Dioecious fig pollinators were poorly represented suggesting more limited dispersal, which could account for higher endemism and vulnerability to catastrophic disturbance in these figs. Diurnal activity and flight height also varied among genera. Most non-pollinating fig wasps were very rare.

Dispersal and fighting in male pollinating fig wasps.

For more than two decades, it has been the dogma that the males of pollinating fig wasps do not fight and that they only mate in their native fig. Their extreme degree of local mating leads to highly female biased sex ratios that should eliminate the benefits of fighting and dispersal by males. Furthermore, males sharing a fig are often brothers, and fighting may be barred by kin selection. Therefore, theory supported the presumed absence of fighting and dispersal in pollinating fig wasp males. However, we report here that in pollinating fig wasps, fighting between brothers evolved at least four and possibly six time, and dispersal by males at least twice. This finding supports the idea that competition between relatives can cancel the ameliorating effects of relatedness. The explanation to this evolutionary puzzle, as well as the consequences of male dispersal and fighting, opens the doors to exciting new research.

Why do fig wasps actively pollinate monoecious figs?

Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.

Speciation in fig pollinators and parasites.

Here we draw on phylogenies of figs and fig wasps to suggest how modes of speciation may be affected by interspecific interactions. Mutualists appear to have cospeciated with their hosts to a greater extent than parasites, which showed evidence of host shifting. However, we also repeatedly encountered a pattern not explained by either cospeciation or host switching. Sister species of fig parasites often attack the same host in sympatry, and differences in ovipositor length suggest that parasite speciation could result from divergence in the timing of oviposition with respect to fig development. These observations on fig parasites are consistent with a neglected model of sympatric speciation.