Putting your sons in the right place: the spatial distribution of fig wasp offspring inside figs

Abstract. 1. Pollinating fig wasps (Hymenoptera, Agaonidae) display sex ratio adjustment, producing less female‐biased combined sex ratios as the number of ovipositing females (foundresses) inside a fig increases. Because males have low mobility, the oviposition sites (galled ovules) chosen by each foundress are likely to have consequences for the mating structure of wasp populations within the figs. 2. In this study, the spatial location of male and female progeny of the pollinating fig wasp Liporrhopalum tentacularis developing within figs of its host plant Ficus montana was examined to investigate two questions: (i) are male and/or female wasp offspring clustered together or interspersed? and (ii) is their distribution affected by whether one or two foundresses are present? Microsatellite markers were used to identify the progeny of different foundresses in dual‐foundress figs. 3. More offspring developed in the central part of the figs, compared with the ostiolar and basal parts, irrespective of foundress number. Neither male nor female wasp offspring were clustered within a fig. 4. The sons of the second foundress to enter a fig were positioned at similar minimum distances to both sibling and non‐sibling females, whereas the sons of the first foundress were closer to their sibling females than to non‐sibling females. If male wasps mate predominantly with females in adjacent galls, then the positioning of sons by the second foundresses is beneficial for them both in terms of reduced sibling mating and because they are provided with ready access to the female progeny of the first foundress.     

Only pollinator fig wasps have males that collaborate to release their females from figs of an Asian fig tree

Male insects rarely collaborate with each other, but pollinator fig wasps (Hymenoptera: Agaonidae) are said to be an exception. Immature fig wasps feed on galled ovules located inside figs, the inflorescences of Ficus species (Moraceae). After mating, adult pollinator males chew communal exit-holes that allow mated females (which are often also their siblings) to escape. Figs also support non-pollinating fig wasps (NPFWs), some of which produce exit-holes independently. We determined whether collaboration between pollinator males (Kradibia tentacularis from Ficus montana) was necessary for the release of their females, and used the relationship between male numbers and likelihood of success to measure the extent of cooperation during exit-hole production. These attributes were then compared with those of an NPFW (Sycoscapter sp.) from the same host plant. Pollinators were more abundant than NPFW, but their more female-biased sex ratio meant male pollinator densities were only slightly higher. Individual males of both species could produce an exit-hole. Single males of the NPFW were just as successful as single male pollinators, but only male pollinators cooperated effectively, becoming more successful as their numbers increased. The lack of cooperation among NPFW may be linked to their earlier period of intense inter-male aggression.     

Genomes of 12 fig wasps provide insights into the adaptation of pollinators to fig syconia

Figs and fig pollinators are one of the few classic textbook examples of obligate pollination mutualism. The specific dependence of fig pollinators on the relatively safe living environment with sufficient food sources in the enclosed fig syconia implies that they are vulnerable to habitat changes. However, there is still no extensive genomic evidence to reveal the evolutionary footprint of this long-term mutually beneficial symbiosis in fig pollinators. In fig syconia, there are also non-pollinator species. The non-pollinator species differ in their evolutionary and life histories from pollinators. We conducted comparative analyses on 11 newly sequenced fig wasp genomes and one previously published genome. The pollinators colonized the figs approximately 66.9 million years ago, consistent with the origin of host figs. Compared with nonpollinators, many more genes in pollinators were subject to relaxed selection. Seven genes were absent in pollinators in response to environmental stress and immune activation. Pollinators had more streamlined gene repertoires in the innate immune system, chemosensory toolbox, and detoxification system. Our results provide genomic evidence for the differentiation between pollinators and nonpollinators. The data suggest that owing to the long-term adaptation to the fig, some genes related to functions no longer required are absent in pollinators.     

Making the most of your pollinators: An epiphytic fig tree encourages its pollinators to roam between figs

Ficus species are characterized by their unusual enclosed inflorescences (figs) and their relationship with obligate pollinator fig wasps (Agaonidae). Fig trees have a variety of growth forms, but true epiphytes are rare, and one example is Ficus deltoidea of Southeast Asia. Presumably as an adaptation to epiphytism, inflorescence design in this species is exceptional, with very few flowers in female (seed‐producing) figs and unusually large seeds. Figs on male (pollinator offspring‐generating) trees have many more flowers. Many fig wasps pollinate one fig each, but because of the low number of flowers per fig, efficient utilization by F. deltoidea''s pollinators depends on pollinators entering several female figs. We hypothesized that it is in the interest of the plants to allow pollinators to re‐emerge from figs on both male and female trees and that selection favors pollinator roaming because it increases their own reproductive success. Our manipulations of Blastophaga sp. pollinators in a Malaysian oil palm plantation confirmed that individual pollinators do routinely enter several figs of both sexes. Entering additional figs generated more seeds per pollinator on female trees and more pollinator offspring on male trees. Offspring sex ratios in subsequently entered figs were often less female‐biased than in the first figs they entered, which reduced their immediate value to male trees because only female offspring carry their pollen. Small numbers of large seeds in female figs of epiphytic F. deltoidea may reflect constraints on overall female fig size, because pollinator exploitation depends on mutual mimicry between male and female figs.     

Mutating away from your enemies: The evolution of mutation rate in a host–parasite system

The rate at which mutations occur in nature is itself under natural selection. While a general reduction of mutation rates is advantageous for species inhabiting constant environments, higher mutation rates can be advantageous for those inhabiting fluctuating environments that impose on-going directional selection. Analogously, species involved in antagonistic co-evolutionary arms races, such as hosts and parasites, can also benefit from higher mutation rates. We use modifier theory, combined with simulations, to investigate the evolution of mutation rate in such a host–parasite system. We derive an expression for the evolutionary stable mutation rate between two alleles, each of whose fitness depends on the current genetic composition of the other species. Recombination has been shown to weaken the strength of selection acting on mutation modifiers, and accordingly, we find that the evolutionarily attracting mutation rate is lower when recombination between the selected and the modifier locus is high. Cyclical dynamics are potentially commonplace for loci governing antagonistic species interactions. We characterize the parameter space where such cyclical dynamics occur and show that the evolution of large mutation rates tends to inhibit cycling and thus eliminates further selection on modifiers of the mutation rate. We then find using computer simulations that stochastic fluctuations in finite populations can increase the size of the region where cycles occur, creating selection for higher mutation rates. We finally use simulations to investigate the model behaviour when there are more than two alleles, finding that the region where cycling occurs becomes smaller and the evolutionarily attracting mutation rate lower when there are more alleles.     

Tracking the elusive history of diversification in plant–herbivorous insect–parasitoid food webs: insights from figs and fig wasps

The food webs consisting of plants, herbivorous insects and their insect parasitoids are a major component of terrestrial biodiversity. They play a central role in the functioning of all terrestrial ecosystems, and the number of species involved is mind‐blowing (Nyman et al. 2015 ). Nevertheless, our understanding of the evolutionary and ecological determinants of their diversity is still in its infancy. In this issue of Molecular Ecology, Sutton et al. ( 2016 ) open a window into the comparative analysis of spatial genetic structuring in a set of comparable multitrophic models, involving highly species‐specific interactions: figs and fig wasps. This is the first study to compare genetic structure using population genetics tools in a fig‐pollinating wasp (Pleistodontes imperialis sp1) and its main parasitoid (Sycoscapter sp.A). The fig‐pollinating wasp has a discontinuous spatial distribution that correlates with genetic differentiation, while the parasitoid bridges the discontinuity by parasitizing other pollinator species on the same host fig tree and presents basically no spatial genetic structure. The full implications of these results for our general understanding of plant–herbivorous insect–insect parasitoids diversification become apparent when envisioned within the framework of recent advances in fig and fig wasp biology.     

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.     

Ability to gall: the ultimate basis of host specificity in fig wasps?

1. Fig trees (Ficus spp.) and their host‐specific pollinator fig wasps (Agaonidae) are partners in an obligate mutualism. Receptive phase figs release specific volatiles to attract their pollinators, and this is generally effective in preventing pollinator species from entering figs of the wrong hosts. 2. If entry is attempted into atypical host figs, then ostiole size and shape and style length may also prevent reproduction. In spite of these barriers, there is increasing evidence that fig wasps enter atypical hosts, and that this can result in hybrid seed and fig wasp offspring. 3. This study examines the basis of pollinator specificity in two dioecious fig species from different geographical areas. Kradibia tentacularis pollinates Ficus montana in Asia. Ficus asperifolia from East Africa is closely related but is pollinated by a different species of Kradibia. 4. In glasshouses, K. tentacularis was attracted to its normal host, F1s and backcrosses, but only rarely entered figs of F. asperifolia. Foundresses were able to lay eggs in hybrids, backcrosses, and F. asperifolia, although flower occupancy was lowest in F. asperifolia figs and intermediate in hybrids. 5. The fig wasp failed to reproduce in female F. montana, male F. asperifolia, and male F1s, and most but not all backcrosses to F. montana. This was a result of the failure to initiate gall production. 6. Host specificity in this fig wasp is strongly influenced by host volatiles, but the ability to gall may be the ultimate determinant of whether it can reproduce.     

Parasitism of a pollinator fig wasp: mortalities are higher in figs with more pollinators,but are not related to local densities of figs

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The dominant exploiters of the fig/pollinator mutualism vary across continents,but their costs fall consistently on the male reproductive function of figs

1. Fig trees (Moraceae: Ficus) are keystone species, whose ecosystem function relies on an obligate mutualism with wasps (Chalcidoidea: Agaonidae) that enter fig syconia to pollinate. Each female flower produces one seed (fig female reproductive function), unless it also receives a wasp egg, in which case it supports a wasp. Fig male reproductive function requires both male flowers and pollinator offspring, which are the only vectors of fig pollen. 2. The mutualism is exploited by other wasps that lay eggs but provide no pollination service. Most of these non‐pollinating fig wasps (NPFWs) do not enter syconia, but lay eggs through the wall with long ovipositors. Some are gall‐makers, while others are parasitoids or lethal inquilines of other wasps. 3. Ficus is pan‐tropical and contains >750 fig species. However, NPFW communities vary across fig lineages and continents and their effects on the mutualism may also vary. This provides a series of natural experiments to investigate how the costs to a keystone mutualism vary geographically. 4. We made the first detailed study of the costs of NPFWs in a fig (Ficus obliqua G. Forst) from the endemic Australasian section Malvanthera. In contrast to the communities associated with section Americana in the New World, wasps from the subfamily Sycoryctinae (Chalcidoidea: Pteromalidae) dominated this community. 5. These sycoryctine wasps have a negative impact on pollinator offspring numbers, but not on seed production. Consequently, while the NPFW fauna varies greatly at high taxonomic levels across continents, we show that the consistent main effect of locally dominant exploiters of the mutualism is to reduce fig male reproductive function.     

Import of proteins into peroxisomes: piggybacking to a new home away from home

Peroxisomes are capable of importing folded and oligomeric proteins. However, it is a matter of dispute whether oligomer import by peroxisomes is the exception or the rule. Here, I argue for a clear distinction between homo-oligomeric proteins that are essentially peroxisomal, and dually localized hetero-oligomers that access the peroxisome by piggyback import, localizing there in limited number, whereas the majority remain in the cytosol. Homo-oligomeric proteins comprise the majority of all peroxisomal matrix proteins. There is evidence that binding by Pex5 in the cytosol can regulate their oligomerization state before import. The hetero-oligomer group is made up of superoxide dismutase and lactate dehydrogenase. These proteins have evolved mechanisms that render import inefficient and retain the majority of proteins in the cytosol.     

Parasitoid and inquiline attack in the galls of four alien, cynipid gall wasps: host switches and the effect on parasitoid sex ratios

1. Four alien cynipid gall wasps of the genus Andricus are established and still spreading in the British Isles. The order, according to the northerliness of their distribution boundary, is: A. corruptrix→A. quercuscalicis→A. lignicola→A. kollari. All four aliens have a sexual generation in spring on Quercus cerris (introduced to Britain) and an agamic generation in autumn on native oak species. 2. For 2 years 1994 and 1995, galls of both generations of the four alien species were sampled at eight sites from the south of England to the north of Scotland to determine the parasitoid and inquiline species that attack the new galls. The spring generations of the invading species shared a parasitoid complex of four pteromalid species. Five species of inquilines and 11 species of parasitoids emerged from the autumn galls. 3. Two colonisation events were recorded for A. lignicola and A. corruptrix. On both occasions, the spring generations were found first at the new sites, indicating that the agamic generation provides the colonisers for these invading species. After colonisation, the galls of both species were attacked by parasitoids in their first season. 4. In spring, the invading species were among the most abundant cynipids at all eight sites. By sampling the whole local community of cynipid galls, it was found that the parasitoid species attacking the spring galls of the invaders seemed to have shifted their attack to the new hosts. 5. The secondary sex ratios of the parasitoid species emerging from the sexual galls of A. quercuscalicis (the smallest of the four) showed a strong and significant male bias at all sites and in both years. Parasitoid emergence from the galls of the sexual generations of the other three species (all about equal in size) was between 60 and 70% male, and variable among sites and between years.     

Faster speciation of fig‐wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum

Even though speciation involving multiple interacting partners, such as plants and their pollinators, has attracted much research, most studies focus on isolated phases of the process. This currently precludes an integrated understanding of the mechanisms leading to cospeciation. Here, we examine population genetic structure across six species‐pairs of figs and their pollinating wasps along an elevational gradient in New Guinea. Specifically, we test three hypotheses on the genetic structure within the examined species‐pairs and find that the hypothesized genetic structures represent different phases of a single continuum, from incipient cospeciation to the full formation of new species. Our results also illuminate the mechanisms governing cospeciation, namely that fig wasps tend to accumulate population genetic differences faster than their figs, which initially decouples the speciation dynamics between the two interacting partners and breaks down their one‐to‐one matching. This intermediate phase is followed by genetic divergence of both partners, which may eventually restore the one‐to‐one matching among the fully formed species. Together, these findings integrate current knowledge on the mechanisms operating during different phases of the cospeciation process. They also reveal that the increasingly reported breakdowns in one‐to‐one matching may be an inherent part of the cospeciation process. Mechanistic understanding of this process is needed to explain how the extraordinary diversity of species, especially in the tropics, has emerged. Knowing which breakdowns in species interactions are a natural phase of cospeciation and which may endanger further generation of diversity seems critical in a constantly changing world.     

Knowing your enemies: Integrating molecular and ecological methods to assess the impact of arthropod predators on crop pests

The importance of natural enemies as the foundation of integrated pest management (IPM) is widely accepted, but few studies conduct the manipulative field experiments necessary to directly quantify their impact on pest populations in this context. This is particularly true for predators. Studying arthropod predator–prey interactions is inherently difficult: prey items are often completely consumed, individual predator–prey interactions are ephemeral (rendering their detection difficult) and the typically fluid or soft‐bodied meals cannot be easily identified visually within predator guts. Serological techniques have long been used in arthropod predator gut‐contents analysis, and current enzyme linked immunosorbent assays (ELISA) are highly specific and sensitive. Recently, polymerase chain reaction (PCR) methods for gut‐contents analysis have developed rapidly and they now dominate the diagnostic methods used for gut‐contents analysis in field‐based research. This work has identified trophic linkages within food webs, determined predator diet breadth and preference, demonstrated the importance of cannibalism and intraguild predation within and between certain taxa, and confirmed the benefits (predator persistence) and potential disadvantages (reduced feeding on pest species) of the availability of alternative nonpest prey. Despite considerable efforts to calibrate gut‐contents assays, these methods remain qualitative. Available techniques for predator gut‐contents analysis can provide rapid, accurate, cost‐effective identification of predation events. As such, they perfectly compliment the ecological methods developed to directly assess predator impacts on prey populations but which are imperfect at identifying the key predators. These diagnostic methods for gut‐contents analysis are underexploited in agricultural research and they are almost never applied in unison with the critical field experiments to measure predator impact. This paper stresses the need for a combined approach and suggests a framework that would make this possible, so that appropriate natural enemies can be targeted in conservation biological control.     

Notes on the prey,nesting behaviour and natural enemies of three Bembix sand wasps (Hymenoptera: Crabronidae) in the Iberian Peninsula

Bembix is a cosmopolitan genus with more than 300 species distributed all over the world. The females of these wasps dig burrows in the ground and hunt for flies to feed their larvae. Current knowledge of the nesting behaviour of most Palaearctic species (around 50) is limited. In this study, we provide data on the nest structure, nesting activity, natural enemies and prey captured by three Bembix sand wasps present on the Iberian Peninsula: B. zonata, B. flavescens bolivari and B. merceti. We also analyze the prey spectrum of the three species, comparing our data with those available from previous studies. B. zonata exhibits the greatest selectivity index (and the narrowest niche width), capturing mainly Syrphidae to provision its nests. B. merceti shows the greatest niche width in comparison with the other two species. The inter-annual differences in the diet of B. merceti are important and are probably due to the ability of this wasp to change from one prey resource to another, depending on its availability.     

Journey to the centre of the cell: Virtual reality immersion into scientific data

Visualization of scientific data is crucial not only for scientific discovery but also to communicate science and medicine to both experts and a general audience. Until recently, we have been limited to visualizing the three‐dimensional (3D) world of biology in 2 dimensions. Renderings of 3D cells are still traditionally displayed using two‐dimensional (2D) media, such as on a computer screen or paper. However, the advent of consumer grade virtual reality (VR) headsets such as Oculus Rift and HTC Vive means it is now possible to visualize and interact with scientific data in a 3D virtual world. In addition, new microscopic methods provide an unprecedented opportunity to obtain new 3D data sets. In this perspective article, we highlight how we have used cutting edge imaging techniques to build a 3D virtual model of a cell from serial block‐face scanning electron microscope (SBEM) imaging data. This model allows scientists, students and members of the public to explore and interact with a “real” cell. Early testing of this immersive environment indicates a significant improvement in students’ understanding of cellular processes and points to a new future of learning and public engagement. In addition, we speculate that VR can become a new tool for researchers studying cellular architecture and processes by populating VR models with molecular data.      

Taking the devil into your mouth: ritualized American weight-loss narratives of morality, pain, and betrayal

Abstract:This article examines narratives of the U.S. Christian weight-loss movement alongside secular U.S. weight-loss narratives and explores how these two movements express similar themes. In particular, I investigate shared themes of sin, the impurity of the body, the body as a temple for the self (a temple that can be defiled), salvation, and the need to prove that one is saved or at least trying to be saved. Through examining stories from individuals who have lost weight and popular dieting advice, I explore how a "spiritual hunger" that is essentially unrelated to physiology but that suggests personal pathology and responsibility is central to mainstream stories of weight loss.     

First report of the fall armyworm,Spodoptera frugiperda (Lepidoptera: Noctuidae), natural enemies from Africa

The fall armyworm (FAW), Spodoptera frugiperda, is a major pest of maize in North and South America. It was first reported from Africa in 2016 and currently established as a major invasive pest of maize. A survey was conducted to explore for natural enemies of the fall armyworm in Ethiopia, Kenya and Tanzania in 2017. Smallholder maize farms were randomly selected and surveyed in the three countries. Five different species of parasitoids were recovered from fall armyworm eggs and larvae, including four within the Hymenoptera and one Dipteran. These species are new associations with FAW and were never reported before from Africa, North and South America. In Ethiopia, Cotesia icipe was the dominant larval parasitoid with parasitism ranging from 33.8% to 45.3%, while in Kenya, the tachinid fly, Palexorista zonata, was the primary parasitoid with 12.5% parasitism. Charops ater and Coccygidium luteum were the most common parasitoids in Kenya and Tanzania with parasitism ranging from 6 to 12%, and 4 to 8.3%, respectively. Although fall armyworm has rapidly spread throughout these three countries, we were encouraged to see a reasonable level of biological control in place. This study is of paramount importance in designing a biological control program for fall armyworm, either through conservation of native natural enemies or augmentative release.