Munetoshi Maruyama

Differential host defense against multiple parasites in ants

Host–parasite interactions are ideal systems for the study of coevolutionary processes. Although infections with multiple parasite species are presumably common in nature, most studies focus on the interactions of a single host and a single parasite. To the best of our knowledge, we present here the first study on the dependency of parasite virulence and host resistance in a multiple parasite system. We evaluated whether the strength of host defense depends on the potential fitness cost of parasites in a system of two Southeast Asian army ant hosts and five parasitic staphylinid beetle species. The potential fitness costs of the parasites were evaluated by their predation behavior on host larvae in isolation experiments. The host defense was assessed by the ants’ aggressiveness towards parasitic beetle species in behavioral studies. We found clear differences among the beetle species in both host–parasite interactions. Particular beetle species attacked and killed the host larvae, while others did not. Importantly, the ants’ aggressiveness was significantly elevated against predatory beetle species, while non-predatory beetle species received almost no aggression. As a consequence of this defensive behavior, less costly parasites are more likely to achieve high levels of integration in the ant society. We conclude that the selection pressure on the host to evolve counter-defenses is higher for costly parasites and, thus, a hierarchical host defense strategy has evolved that depends on the parasites’ impact.

Evidence for social parasitism of early insect societies by Cretaceous rove beetles

The evolution of eusociality in ants and termites propelled both insect groups to their modern ecological dominance. Yet, eusociality also fostered the evolution of social parasitism—an adverse symbiosis, in which the superorganismal colonies formed by these insects are infiltrated by a profusion of invertebrate species that target nest resources. Predominant among these are the aleocharine rove beetles (Staphylinidae), a vast and ecologically diverse subfamily with numerous morphologically and behaviourally specialized socially parasitic lineages. Here, we report a fossil aleocharine, Mesosymbion compactus gen. et sp. nov., in Burmese amber (∼99 million years old), displaying specialized anatomy that is a hallmark of social parasites. Mesosymbion coexisted in the Burmese palaeofauna with stem-group ants and termites that provide the earliest indications of eusociality in both insect groups. We infer that the advent of eusociality led automatically and unavoidably to selection for social parasitism. The antiquity and adaptive flexibility of aleocharines made them among the first organisms to engage in this type of symbiosis.

Behavioral differences between two ant cricket species in Nansei Islands: host-specialist versus host-generalist

Ant crickets (Orthoptera, Myrmecophilidae) are typical ant guests that obtain nourishment from the ants in their nests. Some ant crickets are host-specific, whereas other species are host-generalists. We investigated the behavioral polarization between the specialist cricket Myrmecophilus albicinctus and generalist Myrmecophilus formosanus. In the field, M. albicinctus was found exclusively in nests of Anoplolepis gracilipes (185/185), whereas 62 M. formosanus were found in nests of 9 ant species from 3 subfamilies. Behavioral observations revealed that M. albicinctus could not survive in the absence of A. gracilipes and was killed when it was introduced into colonies of non-host ant species. In addition, M. albicinctus showed intimate behavior, such as trophallaxis, with its host. In contrast, M. formosanus swiftly avoided frequent attacks by host ants, independently took food, and survived well in the absence of ants. Overall, the specialist adapted its behavior and physiology to those of a specific ant host, whereas the generalist adopted versatile parasitic behaviors, such as quick movements. Our findings revealed interspecific polarization in the degree of host dependence and inquiline–host interaction, and they indicate that trade-offs occur between specialization to specific hosts and retention of generalization in order to exploit alternative hosts.

A DNA and morphology based phylogenetic framework of the ant genus Lasius with hypotheses for the evolution of social parasitism and fungiculture

BackgroundAnts of the genus Lasius are ecologically important and an important system for evolutionary research. Progress in evolutionary research has been hindered by the lack of a well-founded phylogeny of the subgenera, with three previous attempts disagreeing. Here we employed two mitochondrial genes (cytochrome c oxidase subunit I, 16S ribosomal RNA), comprising 1,265 bp, together with 64 morphological characters, to recover the phylogeny of Lasius by Bayesian and Maximum Parsimony inference after exploration of potential causes of phylogenetic distortion. We use the resulting framework to infer evolutionary pathways for social parasitism and fungiculture.ResultsWe recovered two well supported major lineages. One includes Acanthomyops, Austrolasius, Chthonolasius, and Lasius pallitarsis, which we confirm to represent a seventh subgenus, the other clade contains Dendrolasius, and Lasius sensu stricto. The subgenus Cautolasius, displaying neither social parasitism nor fungiculture, probably belongs to the second clade, but its phylogenetic position is not resolved at the cutoff values of node support we apply. Possible causes for previous problems with reconstructing the Lasius phylogeny include use of other reconstruction techniques, possibly more prone to instabilities in some instances, and the inclusion of phylogenetically distorting characters.ConclusionBy establishing an updated phylogenetic framework, our study provides the basis for a later formal taxonomic revision of subgenera and for studying the evolution of various ecologically and sociobiologically relevant traits of Lasius, although there is need for future studies to include nuclear genes and additional samples from the Nearctic. Both social parasitism and fungiculture evolved twice in Lasius, once in each major lineage, which opens up new opportunities for comparative analyses. The repeated evolution of social parasitism has been established for other groups of ants, though not for temporary social parasitism as found in Lasius. For fungiculture, the independent emergence twice in a monophyletic group marks a novel scenario in ants. We present alternative hypotheses for the evolution of both traits, with one of each involving loss of the trait. Though less likely for both traits than later evolution without reversal, we consider reversal as sufficiently plausible to merit independent testing.

Cryptic diversity, high host specificity and reproductive synchronization in army ant‐associated Vatesus beetles

Army ants and their arthropod symbionts represent one of the most species‐rich animal associations on Earth, and constitute a fascinating example of diverse host–symbiont interaction networks. However, despite decades of research, our knowledge of army ant symbionts remains fragmentary due to taxonomic ambiguity and the inability to study army ants in the laboratory. Here, we present an integrative approach that allows us to reliably determine species boundaries, assess biodiversity, match different developmental stages and sexes, and to study the life cycles of army ant symbionts. This approach is based on a combination of community sampling, DNA barcoding, morphology and physiology. As a test case, we applied this approach to the staphylinid beetle genus Vatesus and its different Eciton army ant host species at La Selva Biological Station, Costa Rica. DNA barcoding led to the discovery of cryptic biodiversity and, in combination with extensive community sampling, revealed strict host partitioning with no overlap in host range. Using DNA barcoding, we were also able to match the larval stages of all focal Vatesus species. In combination with studies of female reproductive physiology, this allowed us to reconstruct almost the complete life cycles of the different beetle species. We show that Vatesus beetles are highly adapted to the symbiosis with army ants, in that their reproduction and larval development are synchronized with the stereotypical reproductive and behavioural cycles of their host colonies. Our approach can now be used to study army ant‐symbiont communities more broadly, and to obtain novel insights into co‐evolutionary and ecological dynamics in species‐rich host–symbiont systems.

Community Sampling and Integrative Taxonomy Reveal New Species and Host Specificity in the Army Ant-Associated Beetle Genus Tetradonia (Coleoptera, Staphylinidae, Aleocharinae)

Army ant colonies host a diverse community of arthropod symbionts. Among the best-studied symbiont communities are those of Neotropical army ants of the genus Eciton. It is clear, however, that even in these comparatively well studied systems, a large proportion of symbiont biodiversity remains unknown. Even more striking is our lack of knowledge regarding the nature and specificity of these host-symbiont interactions. Here we surveyed the diversity and host specificity of rove beetles of the genus Tetradonia Wasmann, 1894 (Staphylinidae: Aleocharinae). Systematic community sampling of 58 colonies of the six local Eciton species at La Selva Biological Station, Costa Rica, combined with an integrative taxonomic approach, allowed us to uncover species diversity, host specificity, and co-occurrence patterns of symbionts in unprecedented detail. We used an integrative taxonomic approach combining morphological and genetic analyses, to delineate species boundaries. Mitochondrial DNA barcodes were analyzed for 362 Tetradonia specimens, and additional nuclear markers for a subset of 88 specimens. All analyses supported the presence of five Tetradonia species, including two species new to science. Host specificity is highly variable across species, ranging from generalists such as T. laticeps, which parasitizes all six local Eciton species, to specialists such as T. lizonae, which primarily parasitizes a single species, E. hamatum. Here we provide a dichotomous key along with diagnostic molecular characters for identification of Tetradonia species at La Selva Biological Station. By reliably assessing biodiversity and providing tools for species identification, we hope to set the baseline for future studies of the ecological and evolutionary dynamics in these species-rich host-symbiont networks.

Asymmetric hindwing foldings in rove beetles

Significance Rove beetles are known to fold their wings in the most complicated and sophisticated ways that have right–left asymmetric patterns. This asymmetric folding can confer both high deployment capability and high storage efficiency, and therefore has a great deal of potential for engineering applications. However, the detailed folding mechanisms have been unclear because of the difficulty of observing of the folding processes. This study used a high-speed camera to observe the wing folding movements of rove beetles. The results show that these characteristic asymmetrical patterns emerge as a result of simultaneous folding of overlapped wings. The specific crease patterns of respective wings and detailed folding motions in each folding sequence are also described here. Foldable wings of insects are the ultimate deployable structures and have attracted the interest of aerospace engineering scientists as well as entomologists. Rove beetles are known to fold their wings in the most sophisticated ways that have right–left asymmetric patterns. However, the specific folding process and the reason for this asymmetry remain unclear. This study reveals how these asymmetric patterns emerge as a result of the folding process of rove beetles. A high-speed camera was used to reveal the details of the wing-folding movement. The results show that these characteristic asymmetrical patterns emerge as a result of simultaneous folding of overlapped wings. The revealed folding mechanisms can achieve not only highly compact wing storage but also immediate deployment. In addition, the right and left crease patterns are interchangeable, and thus each wing internalizes two crease patterns and can be folded in two different ways. This two-way folding gives freedom of choice for the folding direction to a rove beetle. The use of asymmetric patterns and the capability of two-way folding are unique features not found in artificial structures. These features have great potential to extend the design possibilities for all deployable structures, from space structures to articles of daily use.

A case of Batesian mimicry between a myrmecophilous staphylinid beetle, Pella comes, and its host ant, Lasius (Dendrolasius) spathepus : an experiment using the Japanese treefrog, Hyla japonica as a real predator

Abstract.Some myrmecophilous animals show myrmecomorphy, however, its adaptive significance is still controversial. We investigated a possible benefit of Batesianmimicry between a myrmecophilous staphylinid beetle, Pella comes, and its host ant, Lasius (Dendrolasius) spathepus, by using a common ant predator, the Japanese treefrog, Hyla japonica. In the field, H. japonica were found to feed on numerous ants and other insects, but in laboratory experiments they refused feeding on L. spathepus. L. spathepus was highly repellent to these frogs, while P. comes was potentially palatable. After repeated contacts with L. spathepus which led to its avoidance the treefrogs started to reject P. comes as well . This suggests that myrmecomorphy is beneficial to P. comes, reducing the risk of predation, and that it , may represent a case of Batesian mimicry. may represent a case of Batesian mimicry.

Protosternini (Coleoptera : Hydrophilidae) corroborated as monophyletic and its larva described for the first time: a review of the myrmecophilous genus Sphaerocetum

Abstract. The genus Sphaerocetum Fikáček, 2010 is reviewed on the basis of specimens collected from mixed ant nests shared by Camponotus Mayr, 1861 and Crematogaster Lund, 1831 ants in Peninsular Malaysia. Two new species, S. arboreum, sp. nov. and S. hortulanum, sp. nov., are described. A larva of S. arboreum was collected in the same nest as the adults, implying that it is likely that the entire life cycle takes place inside the ant nest; its association with adults was confirmed by cox1 sequences. It is described in detail and represents the first known larva of the tribe Protosternini. Fragments of four genes (cox1, cox2, 18S and 28S) were amplified for S. arboreum and combined with previously generated data in order to test the position of the genus within the subfamily Sphaeridiinae. The analyses revealed Sphaerocetum as a sister taxon to Protosternum Sharp, 1890, corroborating the monophyly of the tribe Protosternini. Bayesian analysis revealed an alternative hypothesis of the phylogenetic position of the tribe, indicating that Protosternini is a sister-group to Omicrini. This position is supported by the chaetotaxy of the maxillary stipes of the larva, which lacks the increased number of stout setae on the inner face present in all other Sphaeridiinae larvae except Omicrini.

A new genus and species of flightless, microphthalmic Corythoderini (Coleoptera: Scarabaeidae: Aphodiinae) from Cambodia, associated with Macrotermes termites

Eocorythoderus incredibilis, a new genus and new species, of Corythoderini is described. This new species was found in fungus gardens of Macrotermes gilvus (Hagen, 1858) in Angkor Wat, Cambodia. The new taxon is a flightless, microphthalmic species and the first corythoderine associated with Macrotermes Holmgren, 1910. The beetles were observed being carried by worker termites. Eocorythoderus is probably closely related to the genera Corythoderus Klug, 1845 and Paracorythoderus Wasmann, 1918 (also Corythoderini). Some character states shared with the distantly-related termitophilous scarab genus Termitotrox Reichensperger, 1915 (Termitotrogini) are noted, and proposed as convergent.