鸡嗉子榕内传粉小蜂与非传粉小蜂的繁殖稳定共存机制研究

【目的】榕-蜂系统是自然界协同进化和互利共生的典型模型,榕-蜂之间如何实现繁殖分配从而实现稳定共存一直是倍受研究者关注的问题,但对传粉小蜂和非传粉小蜂的繁殖稳定共存研究较少。【方法】本文选取分布在西双版纳地区的雌雄异株榕树鸡嗉子榕Ficus semicordata的雄果,通过对榕果内唯一的传粉小蜂Ceratosolen gravelyi Grandi以及4种非传粉小蜂Philotrypesis dunia Joseph,Apocrypta sp.,Platyneura sp.,Sycoscapter trifemmensis Joseph的产卵时序进行了观察,并对5种小蜂的种群数量进行统计,以及对每种小蜂产卵小花的空间分布、瘿花体积等特征进行了研究。【结果】发现:5种小蜂在产卵时间上存在分离,且传粉小蜂的种群数量远大于其他4种非传粉小蜂的种群数量之和。5种小蜂的瘿花特征也存在差异:瘿花的子房大小不同,且花梗长度即分布空间也有差异,传粉小蜂最接近果腔而非传粉小蜂则更多地利用中层和内层的小花。【结论】结果说明在鸡嗉子榕有限的空间内,5种小蜂通过产卵时间和生长空间的分离,实现了减少竞争以及长期共存的特征,维持了榕-蜂系统的稳定性。     

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.     

Longevity, early emergence and body size in a pollinating fig wasp--implications for stability in a fig-pollinator mutualism

1. Fig trees (Ficus) are pollinated only by agaonid wasps, whose larvae also gall fig ovules. Each ovule develops into either a seed (when pollinated) or a wasp (when an egg is also laid inside) but not both. 2. Ovipositing wasps (foundresses) favour ovules near the centre of the enclosed inflorescence (syconium or 'fig'), leaving ovules near the outer wall to develop into seeds. This spatial stratification of wasps and seeds ensures reproduction in both partners, and thereby enables mutualism persistence. However, the mechanism(s) responsible remain(s) unknown. 3. Theory shows that foundresses will search for increasingly rare inner ovules and ignore outer ovules, as long as ovipositing in outer ovules is sufficiently slow and/or if inner ovules confer greater fitness to wasps. The fig-pollinator mutualism can therefore be stabilized by strong time constraints on foundresses and by offspring fitness gradients over variation in ovule position. 4. Female fig wasps cannot leave their galls without male assistance. We found that females in outer ovules were unlikely to be released. Inner ovules thus have added value to foundresses, because their female offspring are more likely to mate and disperse. 5. For those offspring that did emerge, gall position (inner/outer) and body size did not influence the order in which female pollinators exited syconia, nor did early emerging wasps enjoy increased life spans. 6. We also found that the life spans of female wasps nearly doubled when given access to moisture. We suggest that conflict resolution in the fig-pollinator mutualism may thus be influenced by tropical seasonality, because wasps may be less able to over-exploit ovules in dry periods due to time constraints.     

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.     

Foundress re-emergence and fig permeability in fig tree-wasp mutualisms

Some female pollinating fig wasps (foundresses) re-emerge from figs after oviposition/pollination. We investigated why this occurs in the mutualism between the gynodioecious Ficus montana and Liporrhopalum tentacularis. Re-emergence increased with foundress density in figs and some foundresses oviposited in two male figs, indicating that they re-emerge because of oviposition site limitation. Re-emergence was independent of fig diameter, indicating that permeability is not because of fig age at entry. Rather, as some foundresses also pollinate two female figs we suggest permeability is selected for because it increases pollinator production and/or efficiency (although, potentially opposing these hypotheses, we also found between-tree differences in permeability in male figs). In addition, we show that re-emergence is much more common than previously suspected, and more common from gynodioecious than monoecious fig species. We argue that our findings in F. montana could explain this pattern of incidence.     

钝叶榕(Ficus curtipes)非传粉小蜂交配行为

榕树及其传粉榕小蜂繁殖上相互依存,被认为是生物界中协同进化时间最悠久,相互关系最密切的一对生物;在大多数榕树种类的隐头花序内,除了传粉榕小蜂外,还共存着多种非传粉小蜂,它们的繁殖行为直接影响着榕树和传粉榕小蜂的繁殖和互惠稳定.钝叶榕(Ficus curtipes Corner),是一种雌雄同株的绞杀性榕树.研究在西双版纳热带植物园里共收集钝叶榕100个隐头果内的榕小蜂,获得9493号标本;其中,包括1种传粉小蜂和5种非传粉小蜂,钝叶榕传粉小蜂Eupristina sp.占总数的44.66%,杨氏榕树金小蜂Diaziella yangi 占46.13%,而其它4种非传粉小蜂(Lipothymus sp., Sycobia sp., Philotrypesis sp.和Sycoscopter sp.)仅占9.20%.前3种榕小蜂雌蜂进到果腔产卵,其余3种在果外产卵.观测23个钝叶榕榕果出蜂情况发现,6种榕小蜂在钝叶榕隐头花序内遵循严格的羽化出蜂顺序,首先是Sycobia sp.,次之是Lipothymus sp.,再次之是杨氏榕树金小蜂,最后是钝叶榕传粉小蜂、Philotrypesis sp.和Sycoscopter sp..5种非传粉小蜂的交配场所与雄蜂翅型无关,雄蜂有翅型的杨氏榕树金小蜂大部分交配在果内完成,而且它们的雄蜂为争夺交配机会存在激烈的打斗行为;雄蜂无翅型的Lipothymus sp.有部分雄蜂爬出隐头果,在果壁和附近的叶片背面交配;雄蜂有翅型的Sycobia sp.,其所有交配都发生在果外;Philotrypesis sp.和Sycoscopter sp. 雄蜂均无翅,它们的交配全发生在果内.局域配偶竞争使榕小蜂性比偏雌,杨氏榕树金小蜂雄蜂虽然有翅,但大部分交配发生在榕果内,这将影响其最佳的性比率.因此,依赖雄蜂翅型并不能很好地预测榕小蜂的交配场所和性比率.     

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.     

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.     

大果榕亚组三种榕树传粉榕小蜂核型研究

研究了木瓜榕(Ficus auriculata Loureiro)、苹果榕(F.oligodon Miquel)及未知榕(Ficus sp.)3种榕树传粉榕小蜂的核型。结果表明:3种榕树对应的传粉榕小蜂具有非常相似的核型,染色体数目相同为2n=10,染色体全部为中着丝粒染色体;核型公式2n=2X=10=10M,核型均为Stebbins-1A型。以臂比不对称性系数Dc和相对长度不对称性系数Dt作二维散点图,Ceratosolen emarginatus Mayr(木瓜榕传粉榕小蜂)和C.emarginatus Mayr(苹果榕传粉榕小蜂)具有非常相近的核型不对称系数,核型不对称性大于Ceratosolen sp.(未知榕传粉榕小蜂),显示出两者更近的亲缘关系,而Ceratosolen sp.(未知榕)与前两者亲缘关系较远。此外,比较了Ceratosolen属和Blastophaga属在核型方面的差异,认为染色体数目包括染色体形态能够作为准确区分Ceratosolen属和Blastophaga属的依据,并对Ceratosolen属的核型进化进行了初步探讨。     

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 .     

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。     

The mechanism of sex ratio adjustment in a pollinating fig wasp

Sex ratio strategies in species subject to local mate competition (LMC), and in particular their fit to quantitative theoretical predictions, provide insight into constraints upon adaptation. Pollinating fig wasps are widely used in such studies because their ecology resembles theory assumptions, but the cues used by foundresses to assess potential LMC have not previously been determined. We show that Liporrhopalum tentacularis females (foundresses) use their clutch size as a cue. First, we make use of species ecology (foundresses lay multiple clutches, with second clutches smaller than first) to show that increases in sex ratio in multi-foundress figs occur only when foundresses are oviposition site limited, i.e. that there is no direct response to foundress density. Second, we introduce a novel technique to quantify foundress oviposition sequences and show, consistent with the theoretical predictions concerning clutch size-only strategies, that they produce mainly male offspring at the start of bouts, followed by mostly females interspersed by a few males. We then discuss the implications of our findings for our understanding of the limits of the ability of natural selection to produce 'perfect' organisms, and for our understanding of when different cue use patterns evolve.     

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.     

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.     

Ancient fig wasps indicate at least 34 Myr of stasis in their mutualism with fig trees

Fig wasps and fig trees are mutually dependent, with each of the 800 or so species of fig trees (Ficus, Moraceae) typically pollinated by a single species of fig wasp (Hymenoptera: Agaonidae). Molecular evidence suggests that the relationship existed over 65 Ma, during the Cretaceous. Here, we record the discovery of the oldest known fossil fig wasps, from England, dated at 34 Ma. They possess pollen pockets that contain fossil Ficus pollen. The length of their ovipositors indicates that their host trees had a dioecious breeding system. Confocal microscopy and scanning electron microscopy reveal that the fossil female fig wasps, and more recent species from Miocene Dominican amber, display the same suite of anatomical characters associated with fig entry and pollen-carrying as modern species. The pollen is also typical of modern Ficus. No innovations in the relationship are discernible for the last tens of millions of years.     

Pollinating fig wasps: genetic consequences of island recolonization

The levels of genetic diversity and gene flow may influence the long-term persistence of populations. Using microsatellite markers, we investigated genetic diversity and genetic differentiation in island (Krakatau archipelago, Indonesia) and mainland (Java and Sumatra, Indonesia) populations of Liporrhopalum tentacularis and Ceratosolen bisulcatus, the fig wasp pollinators of two dioecious Ficus (fig tree) species. Genetic diversity in Krakatau archipelago populations was similar to that found on the mainland. Population differentiation between mainland coastal sites and the Krakatau islands was weak in both wasp species, indicating that the intervening 40 km across open sea may not be a barrier for wasp gene flow (dispersal) and colonization of the islands. Surprisingly, mainland populations of the fig waSPS may be more genetically isolated than the islands, as gene flow between populations on the Javan mainland differed between the two wasp species. Contrasting growth forms and relative 'immunity' to the effects of deforestation in their host fig trees may account for these differences.     

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.     

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.     

Restructuring of a mutualism following introduction of Australian fig trees and pollinating wasps to Europe and the USA

Figs and fig-pollinating wasps are obligate mutualists that require each other to complete sexual reproduction. However, landscapers can establish populations of fig trees outside their native ranges by propagation through exported seeds, seedlings or cuttings. Once mature, these trees could be colonized by pollinating wasps and/or various non-pollinating wasps that also develop in figs. In recent decades, the Australian endemic Ficus rubiginosa has been planted widely in the Mediterranean region and in parts of the USA. Observation of ripe fruit production suggested that a pollination mutualism has been re-established by pollinating wasps colonizing trees in the plant’s introduced range. We therefore used sampling of pollinators from mainland Spain, Tenerife and California (USA) and molecular studies to characterize the restructured mutualism and compare it with the native range. In the native range, the plant is pollinated by five wasp species that form the Pleistodontes imperialis complex. However, all wasps in the introduced ranges belonged to just one of these species (P. imperialis sp. 1). Moreover, their mtDNA diversity was close to zero and the sequences clearly link them with the native southern population of this species. None of the?>?20 non-pollinating wasp species from the native range were found in the introduced ranges. In summary, the restructured mutualism has been dramatically simplified, lacking all non-pollinating wasps and all but one pollinator species from the native range. Moreover, the one pollinator species to establish successfully shows a drastic reduction in genetic diversity relative to its source population.     

High incidences and similar patterns of Wolbachia infection in fig wasp communities from three different continents

Abstract Wolbachia are endosymbiotic bacteria that infect numerous arthropod species. Previous studies in Panama and Australia revealed that the majority of fig wasp species harbor Wolbachia infections, but that similar patterns of incidence have evolved independently with different wasp species and Wolbachia strains on the two continents. We found Wolbachia infections in 25/47 species (53%) of fig wasp associated with 25 species of Chinese figs. Phylogenetic analyses of Wolbachia wsp sequences indicated that very similar strains are not obviously found in either closely related or ecologically linked fig wasps species. The extremely high prevalence of Wolbachia in fig wasps (over 50% of species infected) is not constrained by geographical origin and is a recurrent theme of fig wasp/Wolbachia interactions.