Genome‐wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae,Ficus)

The obligate mutualism of figs and fig‐pollinating wasps has been one of the classic models used for testing theories of co‐evolution and cospeciation due to the high species‐specificity of these relationships. To investigate the species‐specificity between figs and fig pollinators and to further understand the speciation process in obligate mutualisms, we examined the genetic differentiation and phylogenetic relationships of four closely related fig‐pollinating wasp species (Blastophaga nipponica, Blastophaga taiwanensis, Blastophaga tannoensis and Blastophaga yeni) in Japan and Taiwan using genome‐wide sequence data, including mitochondrial DNA sequences. In addition, population structure was analysed for the fig wasps and their host species using microsatellite data. The results suggest that the three Taiwanese fig wasp species are a single panmictic population that pollinates three dioecious fig species, which are sympatrically distributed, have large differences in morphology and ecology and are also genetically differentiated. Our results illustrate the first case of pollinator sharing by host shift in the subgenus Ficus. On the other hand, there are strict genetic codivergences between allopatric populations of the two host–pollinator pairs. The possible processes that produce these pollinator‐sharing events are discussed based on the level and pattern of genetic differentiation in these figs and fig wasps.     

One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps

The study of chalcid wasps that live within syconia of fig trees (Moraceae, Ficus ), provides a unique opportunity to investigate the evolution of specialized communities of insects. By conducting cospeciation analyses between figs of section Galoglychia and some of their associated fig wasps, we show that, although host switches and duplication have evidently played a role in the construction of the current associations, the global picture is one of significant cospeciation throughout the evolution of these communities. Contrary to common belief, nonpollinating wasps are at least as constrained as pollinators by their host association in their diversification in this section. By adapting a randomization test in a supertree context, we further confirm that wasp phylogenies are significantly congruent with each other, and build a "wasp community" supertree that retrieves Galoglychia taxonomic subdivisions. Altogether, these results probably reflect wasp host specialization but also, to some extent, they might indicate that niche saturation within the fig prevents recurrent intrahost speciation and host switching. Finally, a comparison of ITS2 sequence divergence of cospeciating pairs of wasps suggests that the diversification of some pollinating and nonpollinating wasps of Galoglychia figs has been synchronous but that pollinating wasps exhibit a higher rate of molecular evolution.     

Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps*

The fig and pollinator wasp obligate mutualism is diverse (～750 described species), ecologically important, and ancient (～80 Ma). Once thought to be an example of strict one‐to‐one cospeciation, current thinking suggests genera of pollinator wasps codiversify with corresponding sections of figs, but the degree to which cospeciation or other processes contribute to the association at finer scales is unclear. Here, we use genome‐wide sequence data from a community of Panamanian strangler figs and associated wasp pollinators to estimate the relative contributions of four evolutionary processes generating cophylogenetic patterns in this mutualism: cospeciation, host switching, pollinator speciation, and pollinator extinction. Using a model‐based approach adapted from the study of gene family evolution, our results demonstrate the importance of host switching of pollinator wasps at this fine phylogenetic and regional scale. Although we estimate a modest amount of cospeciation, simulations reveal the number of putative cospeciation events to be consistent with what would be expected by chance. Additionally, model selection tests identify host switching as a critical parameter for explaining cophylogenetic patterns in this system. Our study demonstrates a promising approach through which the history of evolutionary association between interacting lineages can be rigorously modeled and tested in a probabilistic phylogenetic framework.     

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

Genetic and physiological data suggest demographic and adaptive responses in complex interactions between populations of figs (Ficus pumila) and their pollinating wasps (Wiebesia pumilae)

To study interactions between host figs and their pollinating wasps and the influence of climatic change on their genetic structures, we sequenced cytoplasmic and nuclear genes and genotyped nuclear microsatellite loci from two varieties of Ficus pumila, the widespread creeping fig and endemic jelly fig, and from their pollinating wasps, Wiebesia pumilae, found in Taiwan and on nearby offshore islands. Great divergence in the mitochondrial cytochrome c oxidase subunit I (mtCOI) with no genetic admixture in nuclear markers indicated that creeping‐ and jelly‐fig wasps are genetically distinct. Compared with creeping‐fig wasps, jelly‐fig wasps also showed better resistance under cold (20 °C) than warm (25 and 30 °C) conditions in a survival test, indicating their adaptation to a cold environment, which may have facilitated population expansion during the ice age as shown by a nuclear intron and 10 microsatellite loci. An excess of amino acid divergence and a pattern of too many rare mtCOI variants of jelly‐fig wasps as revealed by computer simulations and neutrality tests implied the effect of positive selection, which we hypothesize was associated with the cold‐adaptation process. Chloroplast DNA of the two fig plants was completely segregated, with signs of genetic admixture in nuclear markers. As creeping‐ and jelly‐fig wasps can pollinate creeping figs, occasional gene flow between the two figs is thus possible. Therefore, it is suggested that pollinating wasps may be playing an active role in driving introgression between different types of host fig.     

榕-传粉小蜂化学通讯机制研究进展

榕属植物与其传粉小蜂组成了高度专一的专性共生关系(榕-蜂共生系统),如此高度紧密的互作关系被认为是驱动两者多样化的关键因素。榕-蜂共生系统主要依靠化学通讯完成相互识别,但目前仍不清楚化学通讯是如何维系现有共生关系并促进物种形成的。结合已有研究,系统梳理了榕-蜂共生系统化学通讯的基础与两者特异性识别的机制,阐述化学通讯在物种和种群层次对维持这一专性传粉关系的重要贡献,进而探讨化学通讯如何在协同成种和宿主转移成种两种模式中介导物种形成。最后,结合生理与多组学等技术展望榕-蜂共生系统的未来研究方向,为深入解析植物与昆虫协同进化的机制以及全球变化下物种的潜在响应模式提供重要参考。     

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.     

Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism

1. Fig pollinating wasps (Agaonidae) enter Ficus inflorescences (figs), oviposit in some of the flowers, and pollinate in the process. Each larva completes its development within a single flower. In most cases, an inflorescence entered by a wasp will represent its only egg‐laying site. The mechanisms that prevent pollinating wasps from exploiting all the flowers inside a fig are not understood. In this study, hypotheses about flower use by pollinating fig wasps were tested by investigating egg deposition patterns in three species. 2. Either one or three wasps were introduced into figs. The figs were then harvested. Serial sections allowed assessment of the presence or absence of a wasp egg in a sample of flowers in each fig. The overall proportion of flowers with eggs and the spatial distribution of eggs were then compared in single wasp figs and three foundress figs. 3. In all species, the proportion of flowers with a wasp egg increased with foundress number but less than three‐fold. 4. In all species, at least in single foundress figs, flowers near the fig cavity were more likely to receive a wasp egg than were flowers near the fig wall. 5. In two species, when the number of foundresses was multiplied by three, there was an increase in the use of flowers near the fig wall, while in the third species, the increase was spread evenly among flowers. 6. Factors affecting wasp egg deposition patterns and the potential of investigating such patterns for studying the stability of the mutualism are discussed.     

非传粉小蜂对榕-蜂共生系统的影响

榕-蜂共生系统是桑科榕属(Ficus)植物与传粉榕小蜂专一互惠形成的生态学关系。但是,也有一些非传粉的小蜂出现在这个系统中,对榕-蜂共生系统可能产生较大的影响。西双版纳的聚果榕(Ficus racemosa)树上主要有5种非传粉小蜂,分别在榕果发育的不同阶段从果外向果内产卵。在传粉榕小蜂进果之前的花前期,Platyneura testace、Apocrypta sp.和P. mayri这3种非传粉小蜂先后到果外产卵繁殖后代,对榕-蜂共生系统造成显著影响,尤其是影响传粉榕小蜂的繁殖。在传粉榕小蜂进果之后的间花期,P. mayri、A. westwoodi和P. agraensis这3种非传粉小蜂相继到果外产卵,它们虽然能减少种子形成和传粉榕小蜂繁殖的数量,但最终没有对榕-蜂共生系统造成显著的影响。造瘿类的P. mayri可在花前期和间花期产卵繁殖,在花前期产卵时它主要是影响传粉榕小蜂的繁殖,而在间花期产卵时它则更多地是影响种子的生产。     

垂叶榕上16种榕小蜂的种群动态

传粉榕小蜂和榕树的互利共生是传粉昆虫与植物间协同进化的典范。在榕果(榕树的隐头状花序)内,还生活着多种非传粉榕小蜂。这些生活在密闭榕果内由传粉榕小蜂和非传粉榕小蜂组成的群落对研究群落生态学有很大价值。然而,对生存在单一榕树的榕果内的所有榕小蜂的种群动态了解很少,特别是缺少相对长期的连续数据。通过野外近3a观察和采样,研究了垂叶榕榕小蜂群落结构和榕小蜂的种群动态。共记录榕小蜂16种;各种榕小蜂根据发生规律可分为常见种和偶见种,Eupristina koningsbergeri,Philotrypesis sp.1,Philotrypesis sp.4,Philotrypesis sp.5,Sycoscapter sp.1,Walkerella benjamini,Walkerella sp.1,Sycophila sp.2,Sycobia sp.2为常见种;Sycobia sp.1,Acophila sp.1,Sycophila sp.1,Ormyrus sp.1等为偶见种。每种榕小蜂在单果上的数量随季节呈波动变化,季节对榕小蜂群落的多样性和均匀性无显著影响。除了传粉榕小蜂外,Sycoscapter sp.1也是优势种类之一。传粉榕小蜂的数量与非传粉榕小蜂总数间呈显著负相关。传粉榕小蜂与非传粉榕小蜂几乎都呈负相关,而与Walkerella sp.1在数量上呈显著正相关。Sycobia sp.2与Sycophila sp.2在同一瘿中出现,数量上呈显著正相关。但其它非传粉榕小蜂种类在数量上的相关性较为复杂,可能是造成各种榕小蜂数量波动的一个原因。     

Maintenance of Specificity in an Isolated Fig

The obligate interaction between figs and their pollinating wasps is often cited as an extraordinary example of reciprocal species specificity and evolutionary cospeciation. However, recent studies have shown that breakdowns in one-to-one specificity are not rare (30–60% of species depending on the locality). Combined with evidence of hybridization in some species, this led researchers to propose that a better evolutionary model was one of groups of genetically well-defined pollinators coevolving with groups of frequently hybridizing figs. Nevertheless, these recent studies still indicate that a majority of fig species have one or more host-specific pollinator. The extent to which specificity barriers in these species are leaky will have important consequences for the evolutionary process in Ficus . At Lambir Hills N.P., Sarawak, a single individual of Ficus acamptophylla has become recently isolated from conspecifics through clearance of its specialized habitat, but adjacent forest has a diverse fig flora, including 16 species with congeneric pollinators. Thus, when this individual flowered I was able to investigate the maintenance of its specificity barriers in the absence of competition from the normal pollinator. Only 1 percent of inflorescences were entered by a single pollinator species, which had very low reproductive success, and no viable seeds were produced. Nonpollinating wasps also failed to reproduce in any of the inflorescences. These results indicate the maintenance of strict specificity barriers in this fig individual.     

Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites

Figs (Ficus spp., Moraceae) and their pollinating wasps form an obligate mutualism, which has long been considered a classic case of coevolution and cospeciation. Figs are also exploited by several clades of nonpollinating wasps, which are parasites of the mutualism and whose patterns of speciation have received little attention. We used data from nuclear and mitochondrial DNA regions to estimate the phylogenies of 20 species of Pleistodontes pollinating wasps and 16 species of Sycoscapter nonpollinating wasps associated with Ficus species in the section Malvanthera. We compare the phylogenies of 15 matched Pleistodontes/Sycoscapter species pairs and show that the level of cospeciation is significantly greater than that expected by chance. Our estimates of the maximum level of cospeciation (50 to 64% of nodes) are very similar to those obtained in other recent studies of coevolved parasitic and mutualistic associations. However, we also show that there is not perfect congruence of pollinator and parasite phylogenies (for any substantial clade) and argue that host plant switching is likely to be less constrained for Sycoscapter parasites than for Pleistodontes pollinators. There is perfect correspondence between two terminal clades of two sister species in the respective phylogenies, and rates of molecular evolution in these pairs are similar.     

榕果挥发物对传粉榕小蜂的吸引作用

榕树 /榕小蜂专一性共生系统的维持 ,与榕树开花期释放的特殊的挥发性化合物以及榕小蜂对其寄主榕树的化学识别和定位紧密相关。研究选取了西双版纳地区常见的 3种榕树 ,即对叶榕 Ficus hispida、木瓜榕 F.auriculata和鸡嗉子榕F.semicordata的榕果作为实验材料 ,利用野外诱捕实验、室内生物检测实验检测传粉榕小蜂 Hymenoptera:ChalcidoidaeAgaonidae对 12种信息化合物及榕果的二氯甲烷浸提物的趋向性反应 ,研究不同榕属植物的传粉榕小蜂对相同的信息化合物的反应差异 ,以及传粉榕小蜂受不同发育时期榕果浸提物吸引的显著性程度。诱捕实验中对叶榕小蜂 Ceratosolen solmsimarchali对香叶醇的趋向性反应显著 ,大果榕小蜂 C.emarginatus对接受期榕果浸提物和芳樟醇都有明显的趋向性反应 ,而对间花期榕果浸提物则无显著反应。嗅觉仪生物检测实验中 ,鸡嗉果榕小蜂 C.gravelyi对香叶醇和松油醇都表现出显著的趋向性反应。结果表明 ,对叶榕、鸡嗉子榕传粉榕小蜂对 12种信息化合物的反应存在一定的差异 ,木瓜榕传粉榕小蜂对香叶醇和木瓜榕接受期榕果浸提物的趋向性反应比间花期榕果强得多     

How to be an ant on figs

Mutualistic interactions are open to exploitation by one or other of the partners and a diversity of other organisms, and hence are best understood as being embedded in a complex network of biotic interactions. Figs participate in an obligate mutualism in that figs are dependent on agaonid fig wasps for pollination and the wasps are dependent on fig ovules for brood sites. Ants are common insect predators and abundant in tropical forests. Ants have been recorded on approximately 11% of fig species, including all six subgenera, and often affect the fig–fig pollinator interaction through their predation of either pollinating and parasitic wasps. On monoecious figs, ants are often associated with hemipterans, whereas in dioecious figs ants predominantly prey on fig wasps. A few fig species are true myrmecophytes, with domatia or food rewards for ants, and in at least one species this is linked to predation of parasitic fig wasps. Ants also play a role in dispersal of fig seeds and may be particularly important for hemi-epiphytic species, which require high quality establishment microsites in the canopy. The intersection between the fig–fig pollinator and ant–plant systems promises to provide fertile ground for understanding mutualistic interactions within the context of complex interaction networks.     

Permeability of receptive fig fruits and its effects on the re‐emergence behaviour of pollinators

1. Figs and pollinating fig wasps provide a model system for studying mutualism. The permeability of the syconium changes during receptivity or between seasons, which may affect the behaviour of pollinators. Fig fruits are permeable during receptivity, and in some species, pollinators can enter and re‐emerge after oviposition/pollination. We studied the relationship between fig permeability and pollinator re‐emergence behaviour with a functional dioecious fig, Ficus hispida and the obligate pollinator Ceratosolen solmsi marchali. 2. The relationship reflects the interaction of figs and pollinators in the mutualism and also the conflicts of interests between the two partners: figs benefit from the enclosed fig fruits which have low permeability, but pollinators benefit from their re‐emergence behaviour, which requires high fig permeability. 3. The results showed that at the end of receptivity, the permeability of fig fruits lowered rapidly with changes to the ostiole structures, and re‐emergence rate was low, with more re‐emerging pollinators trapped in the ostiolar bracts. Our results also showed that in the rainy season, the length of receptivity was shorter and fig permeability was lower. The re‐emergence rates were also lower than those in the dry season. The results elucidated that figs' interests dominated in the conflicts between fig and pollinating wasp. 4. Based on a new criteria which employed the classification of pollinators found dead in the ostiolar bracts and which involved a survey of 6 monoecious and 12 dioecious fig species, we found that re‐emergence behaviour was prevalent among fig species, and was more prevalent in functional dioecious figs than monoecious ones.     

Characterization of microsatellite markers for Sycoscapter nonpollinating fig wasps

We isolated 18 microsatellites from Sycoscapter australis, a nonpollinating fig wasp that develops in figs of Ficus macrophylla, and assessed their variability in 20 wasps. We further optimized nine of these loci for use in three other Sycoscapter species that develop in Ficus rubiginosa figs and assessed their variability in 47-140 wasps per species. These are the first microsatellites developed for nonpollinating fig wasps and show sufficient polymorphism to become important tools in evolutionary and genetical studies of Sycoscapter wasps.     

Biodiversity loss through speciation collapse: Mechanisms,warning signals,and possible rescue*

Speciation is the process that generates biodiversity, but recent empirical findings show that it can also fail, leading to the collapse of two incipient species into one. Here, we elucidate the mechanisms behind speciation collapse using a stochastic individual‐based model with explicit genetics. We investigate the impact of two types of environmental disturbance: deteriorated visual conditions, which reduce foraging ability and impede mate choice, and environmental homogenization, which restructures ecological niches. We find that: (1) Species pairs can collapse into a variety of forms including new species pairs, monomorphic or polymorphic generalists, or single specialists. Notably, polymorphic generalist forms may be a transient stage to a monomorphic population; (2) Environmental restoration enables species pairs to reemerge from single generalist forms, but not from single specialist forms; (3) Speciation collapse is up to four orders of magnitude faster than speciation, while the reemergence of species pairs can be as slow as de novo speciation; (4) Although speciation collapse can be predicted from either demographic, phenotypic, or genetic signals, observations of phenotypic changes allow the most general and robust warning signal of speciation collapse. We conclude that factors altering ecological niches can reduce biodiversity by reshaping the ecosystem's evolutionary attractors.     

Gradual speciation in a global hotspot of plant diversity

The speciation process that underlies recent, rapid radiations of plants is controversial, and suggested mechanisms range from pollinator or ecological niche differentiation to allopatry and nonadaptive divergence. Phylogenetic approaches to locating the most appropriate speciation models have been constrained by the low levels of molecular divergence between recently diverged species, which are typical of recent, rapid radiations. In this issue of Molecular Ecology, Rymer et al. (2010) used coalescence analyses of sequence data and genome scans of Amplified Fragment Length Polymorphism (AFLP) loci to demonstrate that in a species complex in the irid genus Gladiolus, a member of the hyper diverse Cape flora of southern Africa, speciation is a gradual process. Older divergences are genetically more differentiated, and show a greater difference in flowering time and floral morphology, than taxa that diverged more recently. There is no evidence of any abrupt events. Gene flow is limited by shifts in flowering time and floral morphology; thus, by pre-zygotic rather than by post-zygotic mechanisms, these evolved together with the occupation of somewhat different habitats. This research gives the first critical insight into how the remarkable diversity in a diversity hotspot could have arisen. More importantly, it demonstrates that the speciation process in recent, rapid radiations is tractable and can be investigated with suitable genetic tools.     

Digest: Process‐based phylogenetic models provide unique insights into the evolution of mutualistic networks*

Figs and their pollinating fig wasps are a classic example of long‐term obligate associations between different species. Satler et al. use a process‐based model adopted from molecular evolution to identify the major processes that affect cophylogenetic matching between figs and fig wasps. They find that host‐switching is one of the most important evolutionary processes contributing to current cophylogenetic patterns, illustrating the value of probabilistic approaches to studying the evolutionary history of mutualisms.     

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。