The Weaver Wasp: Spinning Fungus into a Nest

Wasp nests range from simple to complex structures made of paper or mud. Here, we show that a Neotropical wasp of the genus Nitela builds its nest entirely by weaving endophytic fungal hyphae and spider silk harvested from the leaves growing in the understory of the rain forest in French Guiana.     

Comparison between the anatomical and morphological structure of leaf blades and foliar domatia in the ant-plant Hirtella physophora (Chrysobalanaceae)

Background and Aims: Myrmecophytes, or ant-plants, are characterized by their abilityto shelter colonies of some ant species in hollow structures,or ant-domatia, that are often formed by hypertrophy of theinternal tissue at specific locations (i.e. trunk, branches,thorns and leaf pouches). In Hirtella physophora (Chrysobalanaceae),the focal species of this study, the ant-domatia consist ofleaf pouches formed when the leaf rolls over onto itself tocreate two spheres at the base of the blade. Methods: The morphological and anatomical changes through which foliarant-domatia developed from the laminas are studied for the firsttime by using fresh and fixed mature leaves from the same H.physophora individuals. Key results: Ant-domatia were characterized by larger extra-floral nectaries,longer stomatal apertures and lower stomatal density. The anatomicalstructure of the domatia differed in the parenchymatous tissuewhere palisade and spongy parenchyma were indistinct; chloroplastdensity was lower and lignified sclerenchymal fibres were morenumerous compared with the lamina. In addition, the domatiawere thicker than the lamina, largely because the parenchymatousand epidermal cells were enlarged. Conclusions: Herein, the morphological and anatomical changes that permitfoliar ant-domatia to be defined as a specialized leaf structureare highlighted. Similarities as well as structural modificationsin the foliar ant-domatia compared with the lamina are discussedfrom botanical, functional and mutualistic points of view. Theseresults are also important to understanding the reciprocal evolutionarychanges in traits and, thus, the coevolutionary processes occurringin insect–plant mutualisms.     

Co‐evolutionary patterns and diversification of ant–fungus associations in the asexual fungus‐farming ant Mycocepurus smithii in Panama

Partner fidelity through vertical symbiont transmission is thought to be the primary mechanism stabilizing cooperation in the mutualism between fungus‐farming (attine) ants and their cultivated fungal symbionts. An alternate or additional mechanism could be adaptive partner or symbiont choice mediating horizontal cultivar transmission or de novo domestication of free‐living fungi. Using microsatellite genotyping for the attine ant Mycocepurus smithii and ITS rDNA sequencing for fungal cultivars, we provide the first detailed population genetic analysis of local ant–fungus associations to test for the relative importance of vertical vs. horizontal transmission in a single attine species. M. smithii is the only known asexual attine ant, and it is furthermore exceptional because it cultivates a far greater cultivar diversity than any other attine ant. Cultivar switching could permit the ants to re‐acquire cultivars after garden loss, to purge inferior cultivars that are locally mal‐adapted or that accumulated deleterious mutations under long‐term asexuality. Compared to other attine ants, symbiont choice and local adaptation of ant–fungus combinations may play a more important role than partner‐fidelity feedback in the co‐evolutionary process of M. smithii and its fungal symbionts.     

Geographical variation in host–ant specificity of the parasitic butterfly Maculinea alcon in Denmark

Abstract  1. Maculinea alcon uses three different species of Myrmica host ants along a north–south gradient in Europe. Based on this geographical variation in host ant use, Elmes et al . (1994) suggested that M. alcon might consist of three or more cryptic species or host races, each using a single and different host-ant species.
2. Population-specific differences in allozyme genotypes of M. alcon in Denmark ( Gadeberg & Boomsma, 1997 ) have suggested that genetically differentiated forms may occur in a gradient across Denmark, possibly in relation to the use of different host ants.
3. It was found that two host-ant species are indeed used as hosts in Denmark, but not in a clear-cut north–south gradient. Furthermore, specificity was not complete for many M. alcon populations. Of five populations investigated in detail, one used primarily M. rubra as a host, another exclusively used M. ruginodis , while the other three populations used both ant species. No population in Denmark used M. scabrinodis as a host, although this species was present in the habitat and is known to be a host in central and southern Europe.
4. In terms of number of parasites per nest and number of nests parasitised, M. rubra seems to be a more suitable host in populations where two host species are used simultaneously. Host-ant species has an influence on caterpillar size but this varies geographically. Analyses of pupae did not, however, show size differences between M. alcon raised in M. rubra and M. ruginodis nests.
5. The geographical mosaic of host specificity and demography of M. alcon in Denmark probably reflects the co-evolution of M. alcon with two alternative host species. This system therefore provides an interesting opportunity for studying details of the evolution of parasite specificity and the dynamics of host-race formation.     

Behavioural and chemical mechanisms behind a Mediterranean ant–ant association

1. Interspecific competition among ants is common, and so is competitive exclusion among dominant ant species. In contrast, specific associations between non‐parasitic ant species are rare, especially in the temperate zones. As an exception, the subordinate ant Camponotus lateralis frequently co‐occurs with the dominant Crematogaster scutellaris but rarely with other dominant ants. 2. This association is one of various associations between Camponotus and Crematogaster species across the world. However, the mechanisms behind these co‐occurences are largely unknown. 3. In the present study, we therefore investigated the association of Ca. lateralis and Cr. scutellaris. We studied the spatial association of the nests, interspecific aggression, both species' cuticular hydrocarbon profiles, and their propensity to follow the other species' pheromone trails. 4. Crematogaster scutellaris usually attacked and displaced the generally submissive Ca. lateralis, but was significantly less aggressive at jointly used trails. Camponotus nests were always in close proximity to Crematogaster nests. 5. The cuticular hydrocarbons of both species consisted of alkanes with chain lengths between C21 and C35. The two species had 25 hydrocarbons in common, including mono‐, di‐, and tetramethyl alkanes. Despite this qualitative similarity, however, the quantitative hydrocarbon composition differed between the two species. 6. Camponotus lateralis followed artificial trails containing trail pheromones of Cr. scutellaris, but the latter did not follow Ca. lateralis trail pheromones. Interspecific trail‐following by Camponotus, but not vice versa, has been observed in another Camponotus–Crematogaster association and may be a more general mechanism that facilitates associations between the two ant genera.     

Manifold aspects of specificity in a nematode–bacterium mutualism

Coevolution in mutualistic symbiosis can yield, because the interacting partners share common interests, to coadaptation: hosts perform better when associated with symbionts of their own locality than with others coming from more distant places. However, as the two partners of a symbiosis might also experience conflicts over part of their life cycle, coadaptation might not occur for all life‐history traits. We investigated this issue in symbiotic systems where nematodes (Steinernema) and bacteria (Xenorhabdus) reproduce in insects they have both contributed to kill. Newborn infective juveniles (IJs) that carry bacteria in their intestine then disperse from the insect cadaver in search of a new host to infect. We ran experiments where nematodes coinfect insects with bacteria that differ from their native symbiont. In both Steinernema carpocapsae/Xenorhabdus nematophila and Steinernema feltiae/Xenorhabdus bovienii symbioses, we detected an overall specificity which favours the hypothesis of a fine‐tuned co‐adaptation process. However, we also found that the life‐history traits involved in specificity strongly differ between the two model systems: when associated with strains that differ too much from their native symbionts, S. carpocapsae has low parasitic success, whereas S. feltiae has low survival in dispersal stage.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

Post‐association barrier to host switching maintained despite strong selection in a novel mutualism

Following a host shift, repeated co‐passaging of a mutualistic pair is expected to increase fitness over time in one or both species. Without adaptation, a novel association may be evolutionarily short‐lived as it is likely to be outcompeted by native pairings. Here, we test whether experimental evolution can rescue a low‐fitness novel pairing between two sympatric species of Steinernema nematodes and their symbiotic Xenorhabdus bacteria. Despite low mean fitness in the novel association, considerable variation in nematode reproduction was observed across replicate populations. We selected the most productive infections, co‐passaging this novel mutualism nine times to determine whether selection could improve the fitness of either or both partners. We found that neither partner showed increased fitness over time. Our results suggest that the variation in association success was not heritable and that mutational input was insufficient to allow evolution to facilitate this host shift. Thus, post‐association costs of host switching may represent a formidable barrier to novel partnerships among sympatric mutualists.     

Estimation of dispersal distances of the obligately plant‐associated ant Crematogaster decamera

1. In obligate symbioses with horizontal transmission, the population dynamics of the partner organisms are highly interdependent. Host population size limits symbiont number, and distribution of partners is restricted by the presence and thus dispersal abilities of their respective partner. The Crematogaster decamera–Macaranga hypoleuca ant–plant symbiosis is obligate for both partners. Host survival depends on colonisation by its ant partner while foundress queens require hosts for colony establishment. 2. An experimental approach and population genetic analyses were combined to estimate dispersal distances of foundresses in their natural habitat in a Bornean primary rainforest. 3. Colonisation frequency was significantly negatively correlated with distance to potential reproductive colonies. Results were similar for seedlings at natural densities as well as for seedlings brought out in the area experimentally. Population genetic analysis revealed significant population differentiation with an F_ST of 0.041 among foundresses (n = 157) located at maximum 2280 m apart. In genetic spatial autocorrelation, genotypes of foundresses were significantly more similar than expected at random below 550 m and less similar above 620 m. Direct estimation of dispersal distances by pedigree analysis yielded an average dispersal distance of 468 m (maximum 1103 m). 4. For ants that disperse on the wing, genetic differentiation at such small spatial scales is unusual. The specific nesting requirements of the queens and the necessity for queens to find a host quickly could lead to colonisation of the first suitable seedling encountered, promoting short dispersal distances. Nonetheless, dispersal distances of C. decamera queens may vary with habitat or host spatial distribution.     

Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs

Endosymbiotic gut bacteria play an essential role in the nutrition of many insects. Most of the nutritional interactions investigated so far involve gammaproteobacterial symbionts, whereas other groups have received comparatively little attention. Here, we report on the localization and the transmission route of the specific actinobacterial symbiont Coriobacterium glomerans from the gut of the red firebug, Pyrrhocoris apterus (Hemiptera: Pyrrhocoridae ). The symbionts were detected by diagnostic PCRs and FISH in the midgut section M3, in the rectum and in feces of the bugs as well as in the hemolymph of some females. Furthermore, adult female bugs apply the symbionts to the surface of the eggs during oviposition, from where they are later taken up by the hatchlings. Surface sterilization of egg clutches generated aposymbiotic insects and thereby confirmed the vertical transmission route via the egg surface. However, symbionts were readily acquired horizontally when the nymphs were reared in the presence of symbiont-containing eggshells, feces, or adult bugs. Using diagnostic PCRs and partial sequencing of the 16S rRNA gene, closely related bacterial symbionts were detected in the cotton stainer bug Dysdercus fasciatus (Hemiptera: Pyrrhocoridae ), suggesting that the symbiosis with Actinobacteria may be widespread among pyrrhocorid bugs.     

Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees

The obligate mutualisms between flowering plants and their seed-parasitic pollinators constitute fascinating examples of interspecific mutualisms, which are often characterized by high levels of species diversity and reciprocal species specificity. The diversification in these mutualisms has been thought to occur through simultaneous speciation of the partners, mediated by tight reciprocal adaptation; however, recent studies cast doubt over this general view. In this study, we examine the diversity and species specificity of Epicephala moths (Gracillariidae) that pollinate Glochidion trees (Phyllanthaceae), using analysis of mitochondrial and nuclear gene sequences. Phylogenetic analysis of Epicephala moths associated with five Glochidion species in Japan and Taiwan reveal six genetically isolated species that are also distinguishable by male genital morphology: (i) two species specific to single host species (G. acuminatum and G. zeylanicum, respectively); (ii) two species that coexist on G. lanceolatum; and (iii) two species that share two, closely-related parapatric hosts (G. obovatum and G. rubrum). Statistical analysis shows that the two species associated with G. lanceolatum are not sister species, indicating the colonization of novel Glochidion host in at least one lineage. Behavioural observations suggest that all six species possess the actively-pollinating habit, thus none of the studied species has become a nonmutualistic 'cheater' that exploits the benefit resulting from pollination by other species. Our results parallel recent findings in ecologically similar associations, namely the fig-fig wasp and yucca-yucca moth mutualisms, and contribute to a more general understanding of the factors that determine ecological and evolutionary outcomes in these mutualisms.     

Assembling a mutualism: ant symbionts locate their host plants by detecting volatile chemicals

In most mutualisms, partners disperse independently of each other. For instance, in ant-plant symbioses, plants disperse as seeds, and ants disperse as winged queens. For an ant-plant mutualism to persist, therefore, queens must be able to locate and colonise host plant saplings. It has been suggested that host plants emit volatile chemical cues that attract dispersing queens, but this has never been demonstrated experimentally. We used a Y-tube olfactometry protocol to test this hypothesis in the tropical understorey antplant Cordia nodosa Lam. (Boraginaceae), which associates with two genera of ants, Azteca (Dolichoderinae) and Allomerus (Myrmicinae). Both genera show significant attraction to the volatiles of C. nodosa over control understorey plant species that do not associate with ants. These results support the hypothesis that ants are attracted to volatiles emitted by their host plant and suggest a key preadaptation that promoted the evolution of ant-plant symbioses. Received 1 July 2005; revised 2 November 2005; accepted 8 November 2005.     

Characterization of polymorphic microsatellites in the castration parasite plant‐ant Allomerus octoarticulatus cf. demerarae (Formicidae: Myrmicinae)

Fifteen microsatellite loci were isolated from the Peruvian tropical plant‐ant Allomerus octoarticulatus cf. demerarae (Hymenoptera: Myrmicinae) and their polymorphism was characterized. High levels of within‐population variation were observed at most loci, with number of alleles ranging from one to 21, and heterozygosity from 0 to 1 per population sample. Cross‐species amplification of these loci was also tested in one other species of the ant genus Allomerus (Allomerus decemarticulatus), displaying similar life history.     

Host specificity and association of Cerambycidae with the physical characteristics of the wood of trees in a tropical dry forest

Few studies test the host specificity of tropical dry forest cerambycids, in this study, we examined the host preferences of the cerambycids of a tropical dry forest in central Mexico and the association of cerambycid richness and abundance with the physical characteristics of the wood of their host plants. Branch segments of 81 species of woody plants were cut and left exposed to allow cerambycids oviposition, and the branches were collected and placed in emergence chambers. We measured the density, decomposition rate, and volume of wood for each branch segment. Fifty-seven species of cerambycids emerged. We categorized the cerambycids by the degree of host specificity: 23% were generalists, 14% were specialists, and for 63% of the data were insufficient to determine specificity. For the first time we report, for the tropical dry forest, preference patterns between Cerambycidae (subfamilies and species) and their host plants (families and species). Physical characteristics of wood, such as density and decomposition rate, were strongly related to the presence of cerambycids. Cerambycidae in this forest use wood resources that decompose at an intermediate rate and are relatively soft. The cerambycids were most often generalists, and specific cerambycid/tree species associations were rare, but close commensal relationships were found at the level of subfamilies and plant families. Cerambycid richness and abundance depend on the type of host, medium decomposed woods, and the great abundance of each individual host in the area.     

A genome scan of diversifying selection in Ophiocordyceps zombie‐ant fungi suggests a role for enterotoxins in co‐evolution and host specificity

Identification of the genes underlying adaptation sheds light on the biological functions targeted by natural selection. Searches for footprints of positive selection, in the form of rapid amino acid substitutions, and the identification of species‐specific genes have proved to be powerful approaches to identifying the genes involved in host specialization in plant‐pathogenic fungi. We used an evolutionary comparative genomic approach to identify genes underlying host adaptation in the ant‐infecting genus Ophiocordyceps, which manipulates ant behaviour. A comparison of the predicted genes in the genomes of species from three species complexes—O. unilateralis, O. australis and O. subramanianii—revealed an enrichment in pathogenesis‐associated functions, including heat‐labile enterotoxins, among species‐specific genes. Furthermore, these genes were overrepresented among those displaying significant footprints of positive selection. Other categories of genes suspected to be important for virulence and pathogenicity in entomopathogenic fungi (e.g., chitinases, lipases, proteases, core secondary metabolism genes) were much less represented, although a few candidate genes were found to evolve under positive selection. An analysis including orthologs from other entomopathogenic fungi in a broader context showed that positive selection on enterotoxins was specific to the ant‐infecting genus Ophiocordyceps. Together with previous studies reporting the overexpression of an enterotoxin during behavioural manipulation in diseased ants, our findings suggest that heat‐labile enterotoxins are important effectors in host adaptation and co‐evolution in the Ophiocordyceps entomopathogenic fungi.     

Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity

We studied the association between the honeydew-producing membracid Guayaquila xiphias and its tending ants in the cerrado savanna of Brazil, during 1992 and 1993. Results showed that ants attack potential enemies of G. xiphias, and that increased ant density near the treehoppers affects the spatial distribution of parasitoid wasps on the host plant, keeping them away from brood-guarding G. xiphias females. Controlled ant-exclusion experiments revealed that ant presence (seven species) reduces the abundance of G. xiphias’ natural enemies (salticid spiders, syrphid flies, and parasitoid wasps) on the host plant. The data further showed that ant-tending not only increased homopteran survival, but also conferred a direct reproductive benefit to G. xiphias females, which may abandon the first brood to ants and lay an additional clutch next to the original brood. Two years of experimental manipulations, however, showed that the degree of protection conferred by tending ants varies yearly, and that at initially high abundance of natural enemies the ant species differ in their effects on treehopper survival. Ant effects on treehopper fecundity also varied with time, and with shifts in the abundance of natural enemies. This is the first study to simultaneously demonstrate conditionality in ant-derived benefits related to both protection and fecundity in an ant-tended Membracidae, and the first to show the combined action of these effects in the same system. Received: 19 October 1999 / Accepted: 14 February 2000     

Host specificity and host recognition in a chemically-defended herbivore, the tenthredinid sawfly Rhadinoceraea nodicornis

The sawfly Rhadinoceraea nodicornis Konow (Hymenoptera: Tenthredinidae) is a member of a closely related group of species, the tribe Phymatocerini, which feed on the Liliales and Ranunculales. It is known to sequester steroid alkaloids from its host plants, species in the genus Veratrum (Liliales: Melanthiaceae), and to use them as a defence against predators. There are known chemical relationships between the hosts of R. nodicornis and hosts of related sawfly species. We tested whether the R. nodicornis larvae would accept hosts of closely- and more distantly-related sawflies, but found that they accepted only plant species in the genus Veratrum. This specificity was apparently innate, as it was independent of early larval experience. A feeding bioassay showed that the steroid alkaloids from Veratrum nigrum were phagostimulatory for R. nodicornis larvae, suggesting that they may be involved in host recognition. We discuss the possibility that the evolution of recognition of specific compounds may represent the mechanism of host radiation within the Phymatocerini.