榕-蜂互惠关系中榕树对未传粉榕小蜂的惩罚效应

为验证榕树与其传粉榕小蜂这一严格的、一对一的互利共生系统中是否存在寄主惩罚效应,作者于2007年在云南省西双版纳热带植物园中对雌雄同株的垂叶榕（Ficus benjamina）进行了单果放蜂实验。将为垂叶榕传粉的榕小蜂（Eupristina koningsbergeri）处理成带粉和不带粉的两组,每组又分一只和两只两个水平,分别放进单个隐头花序果中。结果发现：没有传粉榕小蜂进入的隐头花序果会很快终止发育并脱落;而在放了传粉榕小蜂的隐头花序果里,除少数几个放一只不带粉的外,隐头花序果基本都能完成其生活史。但是,带粉雌蜂繁殖的后代小蜂数量显著高于没有带粉的雌蜂,特别是在放两只蜂的处理中。研究结果说明传粉榕小蜂的主动传粉对其繁殖不是必需的,但是主动传粉能增加其繁殖成功的几率。这些结果预示着寄主惩罚效应在榕-蜂互惠系统中发挥着作用。     

榕树-榕小蜂互惠合作系统中的非对称性博弈

榕树及其传粉榕小蜂是自然界中目前所知道的关系最为紧密的互利共生系统之一。随着研究的深入, 越来越多的证据发现榕树-传粉榕小蜂之间互惠合作的过程中存在着复杂的竞争和对抗关系, 例如榕树与传粉榕小蜂之间对公共资源的竞争、传粉欺骗与宿主对传粉者的惩罚、榕树与传粉小蜂之间的“军备竞赛”等。在相互竞争或者对抗关系中, 双方表现出非对称性相互作用。其非对称性关系主要表现出如下3个特征: (1)收益不对称, 即榕树(宿主)与传粉榕小蜂(共生体)之间在资源利用等方面的实力不对称; (2)榕树与传粉榕小蜂之间的信息不对称; (3)进化速率不对称。这些非对称的相互作用可能导致种群的波动、榕树与传粉榕小蜂相互适应和进化策略的变化。因此, 理解榕树与传粉榕小蜂之间的非对称交互作用有助于理解为什么合作和冲突在互利共生关系中经常能同时存在, 也将有助于解释榕树-传粉榕小蜂种间相互关系和物种的多样性。     

榕小蜂食性分化与榕树－榕小蜂系统稳定性

在榕树与其传粉小蜂组成的互利阿共生系统中,理解传粉小蜂与各种非传粉小蜂如何共存是解决这一系统稳定性维持机制问题的关键之一.生态位分化被普遍认为是传粉小蜂与各种非传粉小蜂共存的最主要动力.而作为生态位分化中最基础的食性分化在这一系统中如何具体实现尚小清楚.2006年12月至2007年6月.我们以聚果榕(Ficus racemosa)为材料,通过对果内6种榕小蜂进行独立放蜂及两两组合定最放蜂,并对传粉小蜂分别进行不携带花粉和不能产卵的技术处理,研究了寄生在聚果榕果内的5种非传粉小蜂的食性及相互关系,分析了在不同季节下寄生蜂与寄主间的相关系数.研究结果表明:在5种非传粉小蜂中,Platyneura testacea和P mayri是造瘿者,能独立刺激子房发育成瘿花,并使果实发育成熟;而 Apocrypta sp、A.westwoodi和P.agraensis只能寄生于某些已发育的虫瘿,为拟寄生者,它们各自分别与P.testacea,P.mayri和传粉小蜂Ceratosolen fusciceps存在着一对一的寄生关系.拟寄生者与寄主间的相关性在不同季节下会显示出不同的结果,这表明过去文献中用物种间的相关系数推理而确定的食性关系可能是不可靠的.对自然采集榕果内的小蜂群落分析表明,传粉小蜂处于优势地位,这说明在自然情况下非传粉小蜂的种群维持在一个较低水平,对榕树-传粉小蜂系统稳定性影响较小,故能与之长期共存.     

Laticifer distribution in fig inflorescence and its potential role in the fig-fig wasp mutualism

Although in Moraceae the presence of laticifers is considered to be a synapomorphy, little is known about the distribution and morphology of this type of secretory structure in the reproductive organs of its species. Ficus, the largest genus of Moraceae, is characterized by an inflorescence known as syconium and by an obligate mutualistic interaction with pollinating wasps. The objectives of the present study were to evaluate the distribution and morphology of laticifers in syconia of 36 species belonging to different Ficus sections and to survey traits of taxonomic and adaptive value for the group. Syconia containing flowers in a receptive state were collected, fixed and processed for anatomical analysis. All species studied have branched laticifers distributed in the syconium receptacle, in the ostiolar bracts and in the pedicel of staminate flowers. Almost all species show laticifers in the pedicel of shorter-styled flowers. Laticifers also occur in the pedicel of longer-styled flowers in most Ficus sections, except F. curtipes (Conosycea section) and more than 75% of the studied species of the Americanae section. Laticifers are observed in the sepals of 25 of the 36 species studied and occasionally in the pistil. The presence of laticifers in the pedicel of shorter-style flowers and its absence in the pistil suggest that the distribution of this secretory structure in the fig flower was selected by pressures imposed by the fig-fig wasp mutualism. The laticifers in the pedicel of shorter-styled flowers may confer protection to the developing wasp larvae against natural enemies. However, the absence of laticifers in the pistil of most Ficus species studied was probably selected by the mutualistic relationship with the agaonid pollinating wasps since the latex could interfere with oviposition through the style, with the larval development of the pollinating fig wasps, and the emergence of pollinator offspring from their galls.     

The roles of the ostiole in the fig-fig wasp mutualism from a morpho-anatomical perspective

Journal of Plant Research - The syconium is the urn-shaped inflorescence shared by all species of the genus Ficus. The orifice at the apex of the syconium is called the ostiole, and it is covered...     

Flowering asynchrony and mating system effects on reproductive assurance and mutualism persistence in fragmented fig-fig wasp populations

? Premise of the study: Plants and animals may experience reproductive Allee effects in fragmented populations, and obligate pollination mutualisms may be especially sensitive to extinction risk via this density-dependent process. In this study we examine how a shift from within-crown reproductive synchrony to asynchrony influences reproductive assurance through contributions to selfing and outcrossing in small, spatially isolated populations of Ficus. ? Methods: The research focuses on the monoecious fig F. petiolaris and consists of phenological analyses and genetic assessments of selfing and outcrossing for populations located in Baja California's Sonoran Desert. ? Key results: Phenological censuses of eight populations revealed within-crown asynchrony in 44% of reproducing trees, with 16% having sufficient overlap of male and female flowering phases to permit selfing via the cycling of pollinating fig wasps within natal trees. In mating system analyses of two of these populations, however, multilocus outcrossing rates (t(m)) were indistinguishable from 1. This result, combined with low levels of inbreeding, indicates selfing to be absent or at best a minor contributor to reproductive assurance. ? Conclusions: The results indicate that the fitness benefits of within-crown asynchrony lie not with selfing, as commonly asserted, but with increased opportunities for outcross pollen transmission and receipt, changing our understanding of the mechanisms by which reproduction is facilitated and extinction risk minimized in naturally fragmented Ficus populations. Given the role of fig fruit as a keystone food resource in many tropical environments, trait variation leading to reproductive assurance in figs, such as within-crown asynchrony, has broader ecosystem-level implications.     

Correction to: The roles of the ostiole in the fig-fig wasp mutualism from a morphoanatomical perspective

Journal of Plant Research -     

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.     

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.     

Asymmetric or diffusive co-evolution generates meta-populations in fig-fig wasp mutualisms

Co-evolutionary theory assumes co-adapted characteristics are a positive response to counter those of another species,whereby co-evolved species reach an evolutionarily stable interaction through bilateral adaptation.However,evidence from the fig-fig wasp mutualistic system implies very different co-evolutionary selection mechanisms,due to the inherent conflict among interacted partners.Fig plants appear to have discriminatively enforced fig wasps to evolve"adaptation characteristics"that provide greater benefit to the fig,and fig wasps appear to have diversified their evolutionary strategies in response to discriminative enforcement by figs and competition among different fig wasp species.In what appears to be an asymmetric interaction,the prosperity of cooperative pollinating wasps should inevitably lead to population increases of parasitic individuals,thus resulting in localized extinctions of pollinating wasps.In response,the sanctioning of parasitic wasps by the fig should lead to a reduction in the parasitic wasp population.The meta-populations created by such asymmetric interactions may result in each population of coevolved species chaotically oscillated,temporally or evolutionarily.     

Precision of host sanctions in the fig tree–fig wasp mutualism: consequences for uncooperative symbionts

Host sanctions that reduce the relative fitness of uncooperative symbionts provide a mechanism that can limit cheating and thus stabilise mutualisms over evolutionary timescales. Sanctions have been demonstrated empirically in several mutualisms. However, if multiple individual symbionts interact with each host, the precision with which individual cheating symbionts are targeted by host sanctions is critical to their short‐ and long‐term effectiveness. No previous empirical study has directly addressed this issue. Here, we report the precision of host sanctions in the mutualism between fig trees and their pollinating wasps. Using field experiments and molecular parentage analyses, we show that sanctions in Ficus nymphaeifolia act at the level of entire figs (syconia), not at the level of the individual flowers within. Such fig‐level sanctions allow uncooperative wasps, which do not bring pollen, to avoid sanctions in figs to which other wasps bring pollen. We discuss the relevance of sanction precision to other mutualisms.     

Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism

Bacterial endosymbionts play essential roles for many organisms, and thus specialized mechanisms have evolved during evolution that guarantee the persistence of the symbiosis during or after host reproduction. The rice seedling blight fungus Rhizopus microsporus represents a unique example of a mutualistic life form in which a fungus harbors endobacteria (Burkholderia sp.) for the production of a phytotoxin. Here we report the unexpected observation that in the absence of endosymbionts, the host is not capable of vegetative reproduction. Formation of sporangia and spores is restored only upon reintroduction of endobacteria. To monitor this process, we succeeded in GFP labeling cultured endosymbionts. We also established a laserbeam transformation technique for the first controlled introduction of bacteria into fungi to observe their migration to the tips of the aseptate hyphae. The persistence of this fungal-bacterial mutualism through symbiont-dependent sporulation is intriguing from an evolutionary point of view and implies that the symbiont produces factors that are essential for the fungal life cycle. Reproduction of the host has become totally dependent on endofungal bacteria, which in return provide a highly potent toxin for defending the habitat and accessing nutrients from decaying plants. This scenario clearly highlights the significance for a controlled maintenance of this fungal-bacterial symbiotic relationship.     

A nectar-secreting gall wasp and ant mutualism: selection and counter-selection shaping gall wasp phenology, fecundity and persistence

Abstract.

• 1 The natural history of a gall wasp including interactions with inquilines, parasites, and a mutualistic ant are examined. The stability of the system is described from the perspective of influences on gall wasp life history characteristics.
• 2 An exclusion experiment demonstrated that the nectar-secreting gall of Disholcaspis perniciosa mediates a mutualism with the tending ant, Formica obscuripes. Survivorship increased from 0% in the absence of ants to 25.3% in their presence, largely due to the exclusion of inquilines.
• 3 Specialized parasites, Eudecatoma spp., attacked before the ant-gall interaction began, when the developing gall was still beneath the host plant (Quercus gambellii) epidermis and ants were not in attendance. They may select for later developing gall wasps, which benefit by having fewer individuals parasitized. However, counter-selection for earlier development may result from decreased gall wasp size, decreased fecundity, and an increase in gall failures resulting from late development.
• 4 Local persistence of the gall wasp population despite increased pressure from inquilines and parasites was attributed to gall wasp escape in time due to polymorphic emergence resulting from diapause. Most individuals emerge at the end of the summer, but approximately 15% remain in the galls as prepupae for 1–5 years.

     

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.     

一种非传粉榕小蜂的繁殖策略及其对榕—蜂互利共生系统的影响

为了解非传粉榕小蜂与榕树—传粉榕小蜂互利共生系统的作用方式和作用强度, 从而揭示它们长期稳定共存的原因, 作者于2008年在西双版纳热带植物园研究了钝叶榕(Ficus curtipes)非传粉榕小蜂Walkerella sp.与榕—蜂互利共生系统的相互关系。我们野外直接观察Walkerella sp.的产卵繁殖行为, 并对Walkerella sp.和传粉榕小蜂进行控制放蜂实验。实验包括4类处理榕果: 传粉榕小蜂单种放蜂果, Walkerella sp.单种放蜂果, Walkerella sp.与传粉榕小蜂混合放蜂果, 自然果。结果表明, Walkerella sp.在榕果外产卵, 并且可以将卵产在多个榕果上。单因素方差分析结果表明: 混合放蜂果和自然果内传粉榕小蜂后代数量差异不大(P = 0.46), 但都显著低于传粉榕小蜂单种放蜂果(P < 0.01); 在传粉榕小蜂单种放蜂果以及混合放蜂果内种子数量不存在显著差异(P = 0.33), 但都显著高于自然果(P < 0.01)。自然果内Walkerella sp.后代数量与传粉榕小蜂数量呈显著的相关关系, 而在混合放蜂果内两者呈低度负相关。Walkerella sp.与种子数量在自然果和混合放蜂果都不存在显著的相关关系。单因素方差分析结果表明, Walk-erella sp.单种放蜂果、混合放蜂果及自然果中Walkerella sp.数量不存在显著差异(P < 0.01)。对自然果内所有种类小蜂的相关分析表明: Walkerella sp.与其他非传粉榕小蜂都不存在显著的相关关系, 这说明不存在寄居或复寄生的非传粉榕小蜂种类控制Walkerella sp.的数量。而Walkerella sp.之所以没有完全利用榕果内的小花资源繁殖后代, 是由于产卵量有限和后代必须依靠传粉榕小蜂雄虫打开苞片口才能离开榕果, 必须给传粉小蜂留下一些繁殖资源。     

Interactions of the ant Crematogaster scutellaris with the fig/fig wasp mutualism

Abstract. 1. A classical example of specialised pollination mutualisms is the relationship between fig trees and their pollinating wasps, in which each partner depends completely on the other for its reproduction; however the fig/fig wasp association is also the target of a great diversity of other species, ranging from specialised parasites to opportunistic foragers, among them ants.
2. The ant community and the sources of ant attraction observed on the Mediterranean fig tree Ficus carica were characterised.
3. A guild of ants attracted by homopterans tended on the plant was distinguished from a second guild composed of two co-dominant ant species ( Crematogaster scutellaris and Pheidole pallidula ) that prey mostly on pollinating wasps, abundant during certain parts of the fig cycle.
4. Foraging workers of C. scutellaris search for prey on the fig inflorescence (syconium), capturing pollinating wasps mostly at the peak of wasp emergence and at a rate estimated to reach 600 prey per day for an entire tree.
5. Detailed study of the predatory sequences displayed under experimental conditions showed that ant workers captured 100% of the pollinating wasps offered, while they captured only 5.5% of the parasitoid wasp specific to the pollinator. The respective impacts of the interaction on ants and on the figs are discussed, as well as several behavioural traits of predation by the dominant ant on pollinators.     

Trade-off between reciprocal mutualists: local resource availability-oriented interaction in fig/fig wasp mutualism

1. The mechanisms that prevent competition (conflict) between the recipient and co-operative actor in co-operative systems remain one of the greatest problems for evolutionary biology. Previous hypotheses suggest that self-restraint, dispersal or spatial constraints can prevent direct competition for local resources or any other common resources, thereby maintaining stable co-operation interactions. In this study, we use the obligate fig-fig-wasp mutualism to examine whether the above mechanisms can maintain stable co-operation sufficiently between figs and fig wasps. 2. Our data on obligate co-operation between figs (Ficus racemosa Linn.) and fig wasps (Ceratoslen fusciceps Mayr) show that the number of viable seeds of figs is positively correlated with the number of pollinator offspring when the number of vacant female flowers is high while the foundress number is low (two foundresses). Meanwhile, they are negatively correlated when the number of vacant female flowers is low and the number of foundresses is increased manually (eight foundresses). The correlation coefficient between viable seeds and wasp offspring (galls) depends on vacant female flower availability. 3. Our data suggest that the interaction between figs and fig wasps is conditional, and that they co-operate when local resource availability is plentiful but are in conflict when local resource availability is limited. The self-restraint, dispersal and spatial heterogeneity previously hypothesized in maintaining stable co-operation cannot sufficiently prevent the symbionts from utilizing more local resources at the expense of the recipients. The conflict, which can disrupt the co-operation interaction, exists after the local resource is saturated with symbionts. The repression of symbiont increase, therefore repressing the utilization of local resources in the conflict period, is crucial in the maintenance and evolution of co-operation.     

生态学系统的空间异质性

空间异质性是生态学系统的一个普遍牧场生,生态学家对它在生态学中的重要性已取得了比以往更深刻的认识。试图从空间异质性的含义,空间异质性与尺度和等级的关系,空间异质性的定量描述,空间异质性对生物和非生物过程的影响,以及空间异质性的动态等5个方面综述了有关空间异质性的生态学研究的新进展。