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As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the bee microbiome, its host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.

Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite's genome.

Abstract Background Recent genomic analyses of arthropod defense mechanisms suggest conservation of key elements underlying responses to pathogens, parasites and stresses. At the center of pathogen-induced immune responses are signaling pathways triggered by the recognition of fungal, bacterial and viral signatures. These pathways result in the production of response molecules, such as antimicrobial peptides and lysozymes, which degrade or destroy invaders. Using the recently sequenced genome of the pea aphid (Acyrthosiphon pisum), we conducted the first extensive annotation of the immune and stress gene repertoire of a hemipterous insect, which is phylogenetically distantly related to previously characterized insects models. Results Strikingly, pea aphids appear to be missing genes present in insect genomes characterized to date and thought critical for recognition, signaling and killing of microbes. In line with results of gene annotation, experimental analyses designed to characterize immune response through the isolation of RNA transcripts and proteins from immune-challenged pea aphids uncovered few immune-related products. Gene expression studies, however, indicated some expression of immune and stress-related genes. Conclusions The absence of genes suspected to be essential for the insect immune response suggests that the traditional view of insect immunity may not be as broadly applicable as once thought. The limitations of the aphid immune system may be representative of a broad range of insects, or may be aphid specific. We suggest that several aspects of the aphid life style, such as their association with microbial symbionts, could facilitate survival without strong immune protection.

Abstract Background Aphids are striking in their prodigious reproductive capacity and reliance on microbial endosymbionts, which provision their hosts with necessary amino acids and provide protection against parasites and heat stress. Perhaps as a result of this bacterial dependence, aphids have limited immune function that may leave them vulnerable to bacterial pathogens. An alternative, non-immunological response that may be available to infected aphids is to increase reproduction, thereby ameliorating fitness loss from infection. Such a response would reduce the need to mount a potentially energetically costly immune response, and would parallel that of other hosts that alter life-history traits when there is a risk of infection. Here we examined whether pea aphids (Acyrthosiphon pisum) respond to immunological challenges by increasing reproduction. As a comparison to the response to the internal cue of risk elicited by immunological challenge, we also exposed pea aphids to an external cue of risk - the aphid alarm pheromone (E)-β-farnesene (EBF), which is released in the presence of predators. For each challenge, we also examined whether the presence of symbionts modified the host response, as maintaining host fitness in the face of challenge would benefit both the host and its dependent bacteria. Results We found that aphids stabbed abdominally with a sterile needle had reduced fecundity relative to control aphids but that aphids stabbed with a needle bearing heat-killed bacteria had reproduction intermediate, and statistically indistinguishable, to the aphids stabbed with a sterile needle and the controls. Aphids with different species of facultative symbiotic bacteria had different reproductive patterns overall, but symbionts in general did not alter aphid reproduction in response to bacterial exposure. However, in response to exposure to alarm pheromone, aphids with Hamiltonella defensa or Serratia symbiotica symbiotic infections increased reproduction but those without a facultative symbiont or with Regiella insecticola did not. Conclusions Overall, our results suggest that pea aphids are able to increase their reproduction in response to specific cues and that symbiont presence sometimes moderates this response. Such increased reproduction in response to risk of death increases the fitness of both aphids and their vertically transmitted symbionts, and since these organisms have high reproductive capacity, slight increases in reproduction could lead to a very large numerical advantage later in the season. Thus both symbiotic partners can benefit by increasing host fecundity under dangerous conditions.

Metabolic costs associated with parasites should not be limited to established infections. Even during initial exposure to questing and attacking parasites, hosts can enact behavioural and physiological responses that could also incur metabolic costs. However, few studies have measured these costs directly. Hence, little is known about metabolic costs arising from parasite exposure.Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure.Here, using the California killifish Fundulus parvipinnis and its brain‐infecting parasite Euhaplorchis californiensis, we quantified how killifish metabolism, behaviour and osmoregulatory phenotype changed upon acute exposure to parasite infectious stages (i.e. cercariae), and with long‐term infection.Exposure to cercariae caused both naïve and long‐term infected killifish to acutely increase their metabolic rate and activity, indicating detection and response to parasite infectious stages. Additionally, these metabolic and behavioural effects were moderately stronger in long‐term infected hosts than naïve killifish, suggesting that hosts may develop learned behavioural responses, nociceptor sensitization and/or acute immune mechanisms to limit new infections.Although established infection altered the metabolic response to parasite exposure, established infection did not alter standard metabolic rate, routine metabolic rate, maximum metabolic rate, aerobic scope or citrate synthase enzyme activity.Unexpectedly, established infection reduced lactate dehydrogenase enzyme activity in killifish brains and relative Na+/K+‐ATPase abundance in gills, suggesting novel mechanisms by which E. californiensis may alter its hosts' behaviour and osmoregulation.Thus, we provide empirical evidence that parasites can disrupt the metabolism of their host both during parasite exposure and after infection is established. This response may be modulated by previous infection history, with probable knock‐on effects for host performance, brain energy metabolism, osmoregulation and ecology. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

The role of biotic interactions in shaping species distributions is a cornerstone of biogeographic theory; yet, it remains elusive. Such interactions are more likely to have an influence on organisms with obligate associations, such as hosts and their parasites. Whereas abiotic conditions may affect the abundance and distribution of parasites in ways similar to free‐living species, attributes of the host could also play a part.Here, we focus on parasitic water mites and their dragonfly and damselfly hosts, and use a hierarchical Bayesian model to examine the relative influence of the abiotic environment and biotic factors such as local host community structure and individual host characteristics on parasite intensity along a broad‐scale environmental gradient. Specifically, we assessed how climate, surrounding vegetation, water chemistry, host community structure as well as the relative abundance and body mass of host species affected the intensity of parasitism on individual hosts along a latitudinal gradient.We found that water chemistry and body mass of the host were the best predictors of variation in parasite intensity among hosts. High parasite intensity was observed in hosts sampled from lakes with high pH, dissolved oxygen and conductivity. Additionally, we found that the intensity of parasitism was strongly influenced by host species identity. In particular, body mass, which shows strong phylogenetic signal, was negatively related to parasite intensity. It may be that larger species, or individuals within species, are more immune to high level of parasitism and/or body mass is correlated with other traits of the host which relate to immunity.Considering both the abiotic environment and attributes of host species is necessary to understand why certain host individuals and locations exhibit more intense parasitism. Amid widespread decline of insect populations world‐wide, some of which are attributed to pathogens and parasites, models predicting rates of parasitism in space and time could become an essential tool for guiding management and conservation efforts. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladas Theropithecus gelada, primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 305 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g. Bos taurus, Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

Increased risk of infectious disease transmission has been proposed as one major cost of group living. While factors corresponding to transmission via exposure to infectious stages and susceptibility to contracting infections upon contact are relatively well understood, both aspects are rarely investigated simultaneously.Here, we assessed the influence of exposure and susceptibility measures on strongyle nematode reinfection after experimental deworming of Barbary macaques (Macaca sylvanus) (n = 57). We investigated impacts of behaviour (social bonds, grooming and ground use) and physiology (faecal glucocorticoids, urinary C‐Peptides, urinary neopterin, gastrointestinal [GI] helminth coinfection) on the likelihood of reinfection, using patch occupancy modelling and information theoretic model selection to determine the best models predicting reinfection patterns.Coinfection was the most consistent risk factor, spending time on presumably contaminated soil, interacting with many partners and forming strong same‐sex bonds also tended to increase infection risk. In contrast, strong social bonds with opposite‐sex partners had a consistently protective effect.Our results indicate that coinfections could serve as an integrative measure of individual disease susceptibility. Furthermore, we show that social contact contributes to both exposure and susceptibility to environmentally transmitted parasites, with the outcome depending on specific interaction patterns. A plain language summary is available for this article. [ABSTRACT FROM AUTHOR]

Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource–consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels).Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons).We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens.Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature‐dependent. In turn, the observed effects of AGW on the functional responses of the hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article. Plain Language Summary [ABSTRACT FROM AUTHOR]

Group living animals are likely to attract more parasites than solitary ones. Parasite loads, however, should also depend on environmental conditions and on host characteristics and behaviours. Previous work has found that social spider colonies harbour communities of kleptoparasitic spiders that forego building their own web and, instead, steal prey from their social host.We examined kleptoparasite loads and host hygiene behaviours in colonies of social and subsocial spiders in the genus Anelosimus along an elevation gradient in eastern Ecuador.We found that kleptoparasite loads declined dramatically with increasing elevation. Host hygiene behaviours, such as debris removal, web repair and interactions with the parasites, also declined with elevation. Within elevations, species with more frequent hygiene behaviours appeared more successful at keeping parasites at bay. Contrary to our predictions, parasite density declined with host nest and colony size.The decline in parasite loads at higher elevations likely reflects a lower rate of energy exchange between colonies and their environments, where colder temperatures mean fewer and smaller prey for colonies to process. The decline in parasite density with host colony size may reflect a decline in the number of accessible prey in larger host colonies, as larger colonies should capture fewer but larger insects due to scaling properties of their three‐dimensional webs.Social immunity, whereby a social host uses social behaviour to fight against parasites, has been studied in eusocial and non‐eusocial insects. This study opens up social spiders as a novel system in which to study how host characteristics interact with environmental factors to affect parasite loads. It also introduces the concept of group‐level immunity to social spiders and suggests a role for colony‐level metabolism in determining ecological patterns in parasitism. A plain language summary is available for this article. Plain Language Summary [ABSTRACT FROM AUTHOR]