Speciation in kleptoparasites of oak gall wasps often correlates with shifts into new tree habitats, tree organs, or gall morphospace.

Host shifts to new plant species can drive speciation for plant-feeding insects, but how commonly do host shifts also drive diversification for the parasites of those same insects? Oak gall wasps induce galls on oak trees and shifts to novel tree hosts and new tree organs have been implicated as drivers of oak gall wasp speciation. Gall wasps are themselves attacked by many insect parasites, which must find their hosts on the correct tree species and organ, but also must navigate the morphologically variable galls with which they interact. Thus, we ask whether host shifts to new trees, organs, or gall morphologies correlate with gall parasite diversification. We delimit species and infer phylogenies for two genera of gall kleptoparasites, Synergus and Ceroptres, reared from a variety of North American oak galls. We find that most species were reared from galls induced by just one gall wasp species, and no parasite species was reared from galls of more than four species. Most kleptoparasite divergence events correlate with shifts to non-ancestral galls. These shifts often involved changes in tree habitat, gall location, and gall morphology. Host shifts are thus implicated in driving diversification for both oak gall wasps and their kleptoparasitic associates.

The rediscovery of the putative ant social parasite Manica parasitica syn. nov. (Hymenoptera: Formicidae) reveals an unexpected endoparasite syndrome.

Parasitism is ubiquitous across the tree of life, and parasites comprise approximately half of all animal species. Social insect colonies attract many pathogens, endo- and ectoparasites, and are exploited by social parasites, which usurp the social environment of their hosts for survival and reproduction. Exploitation by parasites and pathogens versus social parasites may cause similar behavioural and morphological modifications of the host. Ants possess two overlapping syndromes: the endo- and social parasite syndromes. We rediscovered two populations of the putative social parasite Manica parasitica in the Sierra Nevada, and tested the hypothesis that M. parasitica is an independently evolving social parasite. We evaluated traits used to discriminate M. parasitica from its host Manica bradleyi, and examined the morphology of M. parasitica in the context of ant parasitic syndromes. We find that M. parasitica is not a social parasite. Instead, M. parasitica represents cestode-infected M. bradleyi. We propose that M. parasitica should be regarded as a junior synonym of M. bradleyi. Our results emphasize that an integrative approach is essential for unravelling the complex life histories of social insects and their symbionts.

You are what your host eats: The trophic structure and food chain length of a symbiont community are coupled with the plastic diet of the host ant.

Food chain length provides key information on the flow of nutrients and energy in ecosystems. Variation in food chain length has primarily been explained by environmental drivers such as ecosystem size and productivity. Most insights are obtained from theory or aquatic systems, but the importance of these drivers remains largely untested in terrestrial systems. We exploited red wood ant nests markedly differing in size as natural experiments to quantify the drivers of trophic structure and food chain length of their symbiont arthropod communities. Using stable isotopes, we explored the variation in the trophic positions of four symbiont species with the trophic position of the top predator as a proxy for food chain length of the symbiont community. Nest size did not affect food chain length, nor trophic distance between the symbionts. Instead, food chain length and the trophic positions of the symbionts were strongly affected by the host's foraging decisions. When the host diet shifted from predominantly herbivorous to more predacious, the trophic position of the symbionts and food chain length strongly increased. We show for the first time that a food web can be structured by biotic interactions with an engineering species rather than by abiotic environmental variables.

Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics.

Studying the historical biogeography and life history transitions from eusocial colony life to social parasitism contributes to our understanding of the evolutionary mechanisms generating biodiversity in eusocial insects. The ants in the genus Myrmecia are a well-suited system for testing evolutionary hypotheses about how their species diversity was assembled through time because the genus is endemic to Australia with the single exception of the species M. apicalis inhabiting the Pacific Island of New Caledonia, and because at least one social parasite species exists in the genus. However, the evolutionary mechanisms underlying the disjunct biogeographic distribution of M. apicalis and the life history transition(s) to social parasitism remain unexplored. To study the biogeographic origin of the isolated, oceanic species M. apicalis and to reveal the origin and evolution of social parasitism in the genus, we reconstructed a comprehensive phylogeny of the ant subfamily Myrmeciinae. We utilized Ultra Conserved Elements (UCEs) as molecular markers to generate a molecular genetic dataset consisting of 2,287 loci per taxon on average for 66 out of the 93 known Myrmecia species as well as for the sister lineage Nothomyrmecia macrops and selected outgroups. Our time-calibrated phylogeny inferred that: (i) stem Myrmeciinae originated during the Paleocene âˆ¼ 58 Ma ago; (ii) the current disjunct biogeographic distribution of M. apicalis was driven by long-distance dispersal from Australia to New Caledonia during the Miocene âˆ¼ 14 Ma ago; (iii) the single social parasite species, M. inquilina, evolved directly from one of the two known host species, M. nigriceps, in sympatry via the intraspecific route of social parasite evolution; and (iv) 5 of the 9 previously established taxonomic species groups are non-monophyletic. We suggest minor changes to reconcile the molecular phylogenetic results with the taxonomic classification. Our study enhances our understanding of the evolution and biogeography of Australian bulldog ants, contributes to our knowledge about the evolution of social parasitism in ants, and provides a solid phylogenetic foundation for future inquiries into the biology, taxonomy, and classification of Myrmeciinae.

A New Termitophilous Genus of Paederinae Rove Beetles (Coleoptera, Staphylinidae) from the Neotropics and Its Phylogenetic Position.

We describe a new genus and species of Paederinae rove beetles, Ruptor cordatus gen. et sp. nov., which lives in the arboreal nests of the termite Labiotermes labralis (Holmgren, 1906) in the Amazon lowlands of Peru. The morphology of Ruptor gen. nov. is highly derived, apparently due to its close association with the termite host, and thus, morphologically, the genus cannot be classified further than Lathrobiini incertae sedis. In order to address the sister-group relationships of Ruptor gen. nov., we conducted a molecular phylogenetic analysis based on seven gene fragments. The analysis indeed resolved the genus as a member of the tribe Lathrobiini and placed it nested within the informal clade of 'Medonina and allied taxa'. We provide a morphological comparison of the new genus with all known myrmeco- and termitophilous representatives of the subfamily, and to the extent possible, we illustrate other relevant and poorly known Neotropical Paederinae inquilines.

Chemical and behavioural strategies along the spectrum of host specificity in ant-associated silverfish.

BACKGROUND: Host range is a fundamental trait to understand the ecological and evolutionary dynamics of symbionts. Increasing host specificity is expected to be accompanied with specialization in different symbiont traits. We tested this specificity-specialization association in a large group of 16 ant-associated silverfish species by linking their level of host specificity to their degree of behavioural integration into the colony and to their accuracy of chemically imitating the host's recognition system, i.e. the cuticular hydrocarbon (CHC) profile. RESULTS: As expected, facultative associates and host generalists (targeting multiple unrelated ants) tend to avoid the host, whereas host-specialists (typically restricted to Messor ants) were bolder, approached the host and allowed inspection. Generalists and host specialists regularly followed a host worker, unlike the other silverfish. Host aggression was extremely high toward non-ant-associated silverfish and modest to low in ant-associated groups. Surprisingly, the degree of chemical deception was not linked to host specificity as most silverfish, including facultative ant associates, imitated the host's CHC profile. Messor specialists retained the same CHC profile as the host after moulting, in contrast to a host generalist, suggesting an active production of the cues (chemical mimicry). Host generalist and facultative associates flexibly copied the highly different CHC profiles of alternative host species, pointing at passive acquisition (chemical camouflage) of the host's odour. CONCLUSIONS: Overall, we found that behaviour that seems to facilitate the integration in the host colony was more pronounced in host specialist silverfish. Chemical deception, however, was employed by all ant-associated species, irrespective of their degree of host specificity.

Genetic and Usurpation Data Support High Incidence of Bumble Bee Nest Invasion by Socially Parasitic Bumble Bee, Bombus insularis.

Cuckoo bumble bees (Psithyrus) (Lepeletier, 1832) (Hymenoptera: Apidae) are a unique lineage of bees that depend exclusively on a host bumble bee species to provide nesting material, nutritional resources, and labor to rear offspring. In this study, we document usurpation incidence and population genetic data of Bombus insularis (Smith, 1861) (Hymenoptera: Apidae), a bumble bee species in the Psithyrus subgenus, on field-deployed B. huntii colonies in northern Utah, United States. Within 12 d of deploying B. huntii Greene, 1860 (Hymenoptera: Apidae) colonies at two field sites, 13 of the 16 colonies contained at least one established B. insularis female. Although our results demonstrate that field-deployed bumble bee colonies are highly susceptible to B. insularis usurpation, applying a fabricated excluder to prevent the inquiline from invading a colony was 100% effective. Sibship analysis using microsatellite genotype data of 59 B. insularis females estimates that they originated from at least 49 unique colonies. Furthermore, sibship analysis found siblings distributed between the field sites that were 7.04 km apart. Our result suggests that B. insularis females have the capacity to disperse across the landscape in search of host colonies at distances of at least 3.52 km and up to 7.04 km. Our study underscores the detrimental impact B. insularis usurpation has on the host bumble bee colony. As B. insularis significantly impacts the success of bumble bee colonies, we briefly discuss how the utilization of excluders may be useful for commercial bumble bee colonies that are used to pollinate open field crops.

Moving apart together: co-movement of a symbiont community and their ant host, and its importance for community assembly.

BACKGROUND: Species interactions may affect spatial dynamics when the movement of one species is determined by the presence of another one. The most direct species-dependence of dispersal is vectored, usually cross-kingdom, movement of immobile parasites, diseases or seeds by mobile animals. Joint movements of species should, however, not be vectored by definition, as even mobile species are predicted to move together when they are tightly connected in symbiont communities. METHODS: We studied concerted movements in a diverse and heterogeneous community of arthropods (myrmecophiles) associated with red wood ants. We questioned whether joint-movement strategies eventually determine and speed-up community succession. RESULTS: We recorded an astonishingly high number of obligate myrmecophiles outside red wood ant nests. They preferentially co-moved with the host ants as the highest densities were found in locations with the highest density of foraging red wood ants, such as along the network of ant trails. These observations suggest that myrmecophiles resort to the host to move away from the nest, and this to a much higher extent than hitherto anticipated. Interestingly, functional groups of symbionts displayed different dispersal kernels, with predatory myrmecophiles moving more frequently and further from the nest than detritivorous myrmecophiles. We discovered that myrmecophile diversity was lower in newly founded nests than in mature red wood ant nests. Most myrmecophiles, however, were able to colonize new nests fast suggesting that the heterogeneity in mobility does not affect community assembly. CONCLUSIONS: We show that co-movement is not restricted to tight parasitic, or cross-kingdom interactions. Movement in social insect symbiont communities may be heterogeneous and functional group-dependent, but clearly affected by host movement. Ultimately, this co-movement leads to directional movement and allows a fast colonisation of new patches, but not in a predictable way. This study highlights the importance of spatial dynamics of local and regional networks in symbiont metacommunities, of which those of symbionts of social insects are prime examples.

The gall wasp fauna of Iran (Hymenoptera: Cynipidae: Cynipinae): species checklist and biogeographical assessment.

We provide a checklist of the gall wasps (Hymenoptera: Cynipidae: Cynipinae) of Iran, and place these records in a biogeographical perspective on three spatial scales, comprising (i) the Western Palaearctic, (ii) Western Asia (Turkey, the southern Caucasus and the Middle East) and (iii) regions within Iran. We present distribution and biological data for 121 species in 24 genera, representing nine of the 12 known cynipid gall wasp tribes. The most species-rich tribe in Iran is the oak gall wasp tribe Cynipini, with 74 species and 11 genera. Cynipid species richness is highest in the central and northern Zagros, with a distinctively different fauna in the forests along the southern shores of the Caspian Sea. Of the species found in Iran, 63 have distributions that extend westwards far into Europe, and can be considered Western Palaearctic species. Twenty four species comprise a distinct eastern component within the Western Palaearctic, with distributions that include Iran and some or all of Turkey, the Middle East and the Caucasus. Twenty one species are apparently endemic to Iran, with distinct Zagros and Caspian components. We highlight biological and phylogeographic processes that may underlie these patterns.

First record of Cynipidae from Myanmar with description of a new species of Lithosaphonecrus (Hymenoptera: Cynipidae: Synergini).

A new cynipid species, Lithosaphonecrus mindatus Ide, Aung Tanaka, sp. nov., is described from Chin State, northwestern Myanmar. This is the first record of Cynipidae from this country. The new species emerged from a bud gall of Lithocarpus thomsonii. The new species' morphological features closely resemble L. arcoverticus Liu, Zhu Pang, but differ from the latter due to the presence of a broad foveal septum on the mesoscutellum and short triangular median mesoscutal impression and absence of the anteroadmedian signum on the mesoscutum. Partial sequences of cytochrome c oxidase subunit I region (614 bp) show a 14-15% difference between the new species and other congeners.

A new species of Periclistus Foerster, 1869 from China and review of the tribe Diastrophini (Hymenoptera, Cynipoidea, Cynipidae).

A new species of cynipid gall wasps, Periclistus orientalis Pang, Liu & Zhu, sp. nov., is herein described from Hunan, China in the tribe Diastrophini (Hymenoptera: Cynipoidea: Cynipidae). The phylogenetic relationship between Periclistus and all the other Diastrophini genera, except the recently described XestophanopsisPujade-Villar et al., 2019, was analyzed using a fragment of the mitochondrial COI gene and a fragment of the nuclear 28S gene. A taxonomic key to the known genera of Diastrophini and an updated taxonomic key to the known Eastern Palearctic species of Periclistus were provided. In addition, an updated checklist of the known species of the genus from the world is given.

The topology and drivers of ant-symbiont networks across Europe.

Intimate associations between different species drive community composition across ecosystems. Understanding the ecological and evolutionary drivers of these symbiotic associations is challenging because their structure eventually determines stability and resilience of the entire species network. Here, we compiled a detailed database on naturally occurring ant-symbiont networks in Europe to identify factors that affect symbiont network topology. These networks host an unrivalled diversity of macrosymbiotic associations, spanning the entire mutualism-antagonism continuum, including: (i) myrmecophiles - commensalistic and parasitic arthropods; (ii) trophobionts - mutualistic aphids, scale insects, planthoppers and caterpillars; (iii) social parasites - parasitic ant species; (iv) parasitic helminths; and (v) parasitic fungi. We dissected network topology to investigate what determines host specificity, symbiont species richness, and the capacity of different symbiont types to switch hosts. We found 722 macrosymbionts (multicellular symbionts) associated with European ants. Symbiont type explained host specificity and the average relatedness of the host species. Social parasites were associated with few hosts that were phylogenetically highly related, whereas the other symbiont types interacted with a larger number of hosts across a wider taxonomic distribution. The hosts of trophobionts were the least phylogenetically related across all symbiont types. Colony size, host range and habitat type predicted total symbiont richness: ant hosts with larger colony size, a larger distribution range or with a wider habitat range contained more symbiont species. However, we found that different sets of host factors affected diversity in the different types of symbionts. Ecological factors, such as colony size, host range and niche width predominantly determined myrmecophile species richness, whereas host phylogeny was the most important predictor of mutualistic trophobiont, social parasite and parasitic helminth species richness. Lastly, we found that hosts with a common biogeographic history support a more similar community of symbionts. Phylogenetically related hosts also shared more trophobionts, social parasites and helminths, but not myrmecophiles. Taken together, these results suggest that ecological and evolutionary processes structure host specificity and symbiont richness in large-scale ant-symbiont networks, but these drivers may shift in importance depending on the type of symbiosis. Our findings highlight the potential of well-characterized bipartite networks composed of different types of symbioses to identify candidate processes driving community composition.

Two new species of socially parasitic Nylanderia ants from the southeastern United States.

In ants, social parasitism is an umbrella term describing a variety of life-history strategies, where a parasitic species depends entirely on a free-living species, for part of or its entire life-cycle, for either colony founding, survival, and/or reproduction. The highly specialized inquiline social parasites are fully dependent on their hosts for their entire lifecycles. Most inquiline species are tolerant of the host queen in the parasitized colony, forgo producing a worker caste, and invest solely in the production of sexual offspring. In general, inquilines are rare, and their geographic distribution is limited, making it difficult to study them. Inquiline populations appear to be small, cryptic, and they are perhaps ephemeral. Thus, information about their natural history is often fragmentary or non-existent but is necessary for understanding the socially parasitic life history syndrome in more detail. Here, we describe two new species of inquiline social parasites, Nylanderia deyrupi sp. nov. and Nylanderia parasitica sp. nov., from the southeastern United States, parasitizing Nylanderia wojciki and Nylanderia faisonensis, respectively. The formicine genus Nylanderia is large and globally distributed, but until the recent description of Nylanderia deceptrix, social parasites were unknown from this genus. In addition to describing the new social parasite species, we summarize the fragmentary information known about their biology, present a key to both the queens and the males of the Nylanderia social parasites, and discuss the morphology of the social parasites in the context of the inquiline syndrome.

The brood parasite's guide to inclusive fitness theory.

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

An early and mysterious histerid inquiline from Cretaceous Burmese amber (Coleoptera, Histeridae).

We describe a new genus and species of Histeridae from Upper Cretaceous Burmese amber, Amplectister tenax Caterino & Maddison, gen. & sp. n. This species represents the third known Cretaceous histerid, which, like the others, is highly distinct and cannot easily be placed to subfamily. It exhibits prosternal characters in common with Saprininae, but other characters appear inconsistent with this possibility. The abdominal venter is strongly concave, and the hind legs are enlarged and modified for grasping. We hypothesize that this represents the earliest example in Histeridae of modifications for phoresy on social insects.

The cephalic labial gland secretions of two socially parasitic bumblebees Bombus hyperboreus (Alpinobombus) and Bombus inexspectatus (Thoracobombus) question their inquiline strategy.

Social parasitic Hymenopterans have evolved morphological, chemical, and behavioral adaptations to overcome the sophisticated recognition and defense systems of their social host to invade host nests and exploit their worker force. In bumblebees, social parasitism appeared in at least 3 subgenera independently: in the subgenus Psithyrus consisting entirely of parasitic species, in the subgenus Alpinobombus with Bombus hyperboreus, and in the subgenus Thoracobombus with B. inexspectatus. Cuckoo bumblebee males utilize species-specific cephalic labial gland secretions for mating purposes that can impact their inquiline strategy. We performed cephalic labial gland secretions in B. hyperboreus, B. inexspectatus and their hosts. Males of both parasitic species exhibited high species specific levels of cephalic gland secretions, including different main compounds. Our results showed no chemical mimicry in the cephalic gland secretions between inquilines and their host and we did not identify the repellent compounds already known in other cuckoo bumblebees.

Taxonomy and natural history of the myrmecophilous genus Clinterocera Motschulsky, 1858 (Coleoptera: Scarabaeidae: Cetoniinae) from China and adjacent regions: revision of the C. jucunda species group.

The Clinterocera jucunda species group of the genus Clinterocera Motschulsky, 1858 is revised. Fourteen species are recognized within this group, including five new species described herein: C. brevifasciata Xu Qiu, new species from northern Vietnam and China; C. krikkeni Xu Qiu, new species from southwestern China; C. sinensis Xu Qiu, new species from southern China; C. velutina Xu Qiu, new species from Hainan, China; and C. vietnamensis Xu Qiu, new species from central Vietnam and Laos. Clinterocera nigra (Kano, 1931) is elevated to the species level. Clinterocera donckieri (Bourgoin, 1924) revised status is revalidated from the synonymy with C. davidis (Fairmaire, 1878). Two new synonyms are proposed based on examination of types and additional specimens: C. humeralis (Moser, 1902) new synonym and C. cervenkai Krajcík, 2012 new synonym are placed as junior synonyms of C. jucunda (Westwood, 1873) and C. donckieri, respectively. Lectotypes are designated for C. davidis and C. humeralis. Diagnoses and colored illustrations of most species are provided, including other four rare species, C. bicolor (Nonfried, 1893), C. ishikawai (Kurosawa, 1973), C. raui (Paulian, 1961), and C. yunnana (Moser, 1911). A key and a detailed description for the species group are presented. Male genitalia, intraspecific variations, new distribution records, and natural history are given for most species. The relationship between Clinterocera and ants is discussed.

Food-web structure of willow-galling sawflies and their natural enemies across Europe.

Communities consist of species and their interactions. They can thus be described as networks, with species as nodes and interactions as links. Within such networks, the diversity of nodes and the distribution of links may affect patterns of energy transfer between trophic levels, the dynamics of the system, and the outcome in terms of ecosystem functioning. To date, most descriptions of networks have focused on single or relatively few sites, and have oftentimes been built on poorly resolved nodes and links. Yet, comparisons of local interaction networks reveal variation in space and in time, thus spurring interest in methods and theory for understanding patterns, drivers, and consequences of this variation. Progress in this field relies on access to replicate samples of comparable food webs across large spatiotemporal scales, resolved to species rather than to compound nodes. Due to the massive efforts required, high-quality data sets are still scarce. We created a data set on a single community type sampled across Europe: willow species (Salix), willow-galling sawflies (Hymenoptera: Tenthredinidae: Nematinae: Euurina), and their natural enemies (hymenopteran parasitoids and coleopteran, lepidopteran, dipteran, and hymenopteran inquilines). Each sample was referenced in space and time, and each node resolved with the highest possible resolution, including taxonomic affinity, gall type (for herbivores), and mode of parasitism (for natural enemies). Galler survival and link structure were resolved by dissection and rearing of gall inhabitants. In total, the data set is based on 641 site visits over 29 years, and on 165,424 galls representing 96 herbivore nodes and 52 plant nodes. The dissections and rearings yielded 42,129 natural enemies belonging to 126 species, and revealed 1,173 different links. The spatiotemporal and taxonomic resolution of these data make them amenable to analyses of both ecological and evolutionary processes of network assembly. Thus, this data set will facilitate testing of important hypotheses in recent community theory, concerning, e.g., the sampling effort needed to adequately describe interaction structure within ecological communities, the impact of environmental conditions and biotic filters on the distribution of species and their interactions, and the relationship between the global "metaweb" and its local realizations.

Dipteran larvae and microbes facilitate nutrient sequestration in the Nepenthes gracilis pitcher plant host.

The fluid-containing traps of Nepenthes carnivorous pitcher plants (Nepenthaceae) are often inhabited by organisms known as inquilines. Dipteran larvae are key components of such communities and are thought to facilitate pitcher nitrogen sequestration by converting prey protein into inorganic nitrogen, although this has never been demonstrated in Nepenthes Pitcher fluids are also inhabited by microbes, although the relationship(s) between these and the plant is still unclear. In this study, we examined the hypothesis of digestive mutualism between N. gracilis pitchers and both dipteran larvae and fluid microbes. Using dipteran larvae, prey and fluid volumes mimicking in situ pitcher conditions, we conducted in vitro experiments and measured changes in available fluid nitrogen in response to dipteran larvae and microbe presence. We showed that the presence of dipteran larvae resulted in significantly higher and faster releases of ammonium and soluble protein into fluids in artificial pitchers, and that the presence of fluid microbes did likewise for ammonium. We showed also that niche segregation occurs between phorid and culicid larvae, with the former fragmenting prey carcasses and the latter suppressing fluid microbe levels. These results clarify the relationships between several key pitcher-dwelling organisms, and show that pitcher communities facilitate nutrient sequestration in their host.