This book analyzes for the first time how parasites shape the biology of social insects: the ants, wasps, bees, and termites. Paul Schmid-Hempel provides an overview of the existing knowledge of ...parasites in social insects. Current ideas are evaluated using a broad database, and the role of parasites for the evolution and maintenance of the social organization and biology of insects is carefully scrutinized. In addition, the author develops new insights, especially in his examination of the intricate relationships between parasites and their social hosts through the rigorous use of evolutionary and ecological concepts. Schmid-Hempel identifies gaps in our knowledge about parasites in social insects and uses models to develop new questions for future research. In addition, issues that are usually considered separately--such as division of labor, genetics, immunology, and epidemiology--are placed in a common framework to analyze two of the most successful adaptations of life: parasitism and sociality. This work will appeal not only to practitioners in the fields of behavioral ecology and sociobiology, but also to others interested in host-parasite relationships or in social organisms, such as apiculturists struggling to overcome the problems arising from mite infestations of honeybee colonies.
Invertebrates lack the cellular and physiological machinery of the adaptive immune system, but show specificity in their immune response and immune priming. Functionally, immune priming is comparable ...to immune memory in vertebrates. Individuals that have survived exposure to a given parasite are better protected against subsequent exposures. Protection may be cross-reactive, but demonstrations of persistent and specific protection in invertebrates are increasing. This immune priming can cross generations ("trans-generational" immune priming), preparing offspring for the prevailing parasite environment. While these phenomena gain increasing support, the mechanistic foundations underlying such immune priming, both within and across generations, remain largely unknown. Using a transcriptomic approach, we show that exposing bumblebee queens with an injection of heat-killed bacteria, known to induce trans-generational immune priming, alters daughter (worker) gene expression. Daughters, even when unexposed themselves, constitutively express a core set of the genes induced upon direct bacterial exposure, including high expression of antimicrobial peptides, a beta-glucan receptor protein implicated in bacterial recognition and the induction of the toll signaling pathway, and slit-3 which is important in honeybee immunity. Maternal exposure results in a distinct upregulation of their daughters' immune system, with a signature overlapping with the induced individual response to a direct exposure. This will mediate mother-offspring protection, but also associated costs related to reconfiguration of constitutive immune expression. Moreover, identification of conserved immune pathways in memory-like responses has important implications for our understanding of the innate immune system, including the innate components in vertebrates, which share many of these pathways.
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Parasites do not always harm their hosts because the immune system keeps an infection at bay. Ironically, the cost of using immune defenses could itself reduce host fitness. This indirect cost of ...parasitism is often not visible because of compensatory resource intake. Here, workers of the bumblebee, Bombus terrestris, were challenged with lipopolysaccharides and micro-latex beads to induce their immune system under starvation (i.e., not allowing compensatory intake). Compared with controls, survival of induced workers was significantly reduced (by 50 to 70%).
The bumblebee Bombus terrestris is commonly infected by a trypanosomatid gut parasite Crithidia bombi. This system shows a striking degree of genetic specificity where host genotypes are susceptible ...to different genotypes of parasite. To a degree, variation in host gene expression underlies these differences, however, the effects of standing genetic variation has not yet been explored. Here we report on an extensive experiment where workers of twenty colonies of B. terrestris were each infected by one of twenty strains of C. bombi. To elucidate the host's genetic bases of susceptibility to infection (measured as infection intensity), we used a low-coverage (~2 x) genome-wide association study (GWAS), based on angsd, and a standard high-coverage (~15x) GWAS (with a reduced set from a 8 x 8 interaction matrix, selected from the full set of twenty). The results from the low-coverage approach remained ambiguous. The high-coverage approach suggested potentially relevant genetic variation in cell surface and adhesion processes. In particular, mucin, a surface mucoglycoprotein, potentially affecting parasite binding to the host gut epithelia, emerged as a candidate. Sequencing the gut microbial community of the same bees showed that the abundance of bacterial taxa, such as Gilliamella, Snodgrassella, or Lactobacillus, differed between 'susceptible' and 'resistant' microbiota, in line with earlier studies. Our study suggests that the constitutive microbiota and binding processes at the cell surface are candidates to affect infection intensity after the first response (captured by gene expression) has run its course. We also note that a low-coverage approach may not be powerful enough to analyse such complex traits. Furthermore, testing large interactions matrices (as with the full 20 x 20 combinations) for the effect of interaction terms on infection intensity seems to blur the specific host x parasite interaction effects, likely because the outcome of an infection is a highly non-linear process dominated by variation in individually different pathways of host defence (immune) responses.
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Antimicrobial peptides (AMPs) and proteins are important components of innate immunity against pathogens in insects. The production of AMPs is costly owing to resource-based trade-offs, and ...strategies maximizing the efficacy of AMPs at low concentrations are therefore likely to be advantageous. Here, we show the potentiating functional interaction of co-occurring insect AMPs (the bumblebee linear peptides hymenoptaecin and abaecin) resulting in more potent antimicrobial effects at low concentrations. Abaecin displayed no detectable activity against Escherichia coli when tested alone at concentrations of up to 200 μM, whereas hymenoptaecin affected bacterial cell growth and viability but only at concentrations greater than 2 μM. In combination, as little as 1.25 μM abaecin enhanced the bactericidal effects of hymenoptaecin. To understand these potentiating functional interactions, we investigated their mechanisms of action using atomic force microscopy and fluorescence resonance energy transfer-based quenching assays. Abaecin was found to reduce the minimal inhibitory concentration of hymenoptaecin and to interact with the bacterial chaperone DnaK (an evolutionarily conserved central organizer of the bacterial chaperone network) when the membrane was compromised by hymenoptaecin. These naturally occurring potentiating interactions suggest that combinations of AMPs could be used therapeutically against Gram-negative bacterial pathogens that have acquired resistance to common antibiotics.
Common triggers include the peptidoglycan recognition proteins, gram-negative binding proteins, Toll-like receptors (TLRs), nucleotide-binding domain leucin-rich repeats (NLRs), and the cyclic ...GMP-AMP synthase (cGAS) system that detects double-stranded DNA (dsDNA) 1, 2. Fast, error-prone triggers of innate immunity are balanced by slower-acting negative regulators that provide a more accurate assessment of invasion The need for speed in immune response 11 demands a low threshold for triggering the immune cascade, which inevitably leads to many errors. Numerous noncoding micro-RNAs (miRNAs) regulate innate immunity, including the Toll cascade in defense against gram-negative bacteria 18, modification of type I IFN regulation 17, 19, immune cell differentiation 20, and repression of the NLR triggers and their immune cascade 21, 22. ...Leishmania exploits a negative TLR regulator to suppress production of key proinflammatory cytokines 28, viruses manipulate post-translational modifications that normally prevent aberrant responses 29, and many microbes interfere with (negative) receptor crosstalk that normally adjusts immune responses 30.
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Trypanosomatids (Trypanosomatidae, Kinetoplastida) are flagellated protozoa containing many parasites of medical or agricultural importance. Among those, Crithidia bombi and C. expoeki, are common ...parasites in bumble bees around the world, and phylogenetically close to Leishmania and Leptomonas. They have a simple and direct life cycle with one host, and partially castrate the founding queens greatly reducing their fitness. Here, we report the nuclear genome sequences of one clone of each species, extracted from a field-collected infection. Using a combination of Roche 454 FLX Titanium, Pacific Biosciences PacBio RS, and Illumina GA2 instruments for C. bombi, and PacBio for C. expoeki, we could produce high-quality and well resolved sequences. We find that these genomes are around 32 and 34 MB, with 7,808 and 7,851 annotated genes for C. bombi and C. expoeki, respectively-which is somewhat less than reported from other trypanosomatids, with few introns, and organized in polycistronic units. A large fraction of genes received plausible functional support in comparison primarily with Leishmania and Trypanosoma. Comparing the annotated genes of the two species with those of six other trypanosomatids (C. fasciculata, L. pyrrhocoris, L. seymouri, B. ayalai, L. major, and T. brucei) shows similar gene repertoires and many orthologs. Similar to other trypanosomatids, we also find signs of concerted evolution in genes putatively involved in the interaction with the host, a high degree of synteny between C. bombi and C. expoeki, and considerable overlap with several other species in the set. A total of 86 orthologous gene groups show signatures of positive selection in the branch leading to the two Crithidia under study, mostly of unknown function. As an example, we examined the initiating glycosylation pathway of surface components in C. bombi, finding it deviates from most other eukaryotes and also from other kinetoplastids, which may indicate rapid evolution in the extracellular matrix that is involved in interactions with the host. Bumble bees are important pollinators and Crithidia-infections are suspected to cause substantial selection pressure on their host populations. These newly sequenced genomes provide tools that should help better understand host-parasite interactions in these pollinator pathogens.
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In many systems, host–parasite evolutionary dynamics have led to the emergence and maintenance of diverse parasite and host genotypes within the same population. Genotypes vary in key attributes: ...Parasite genotypes vary in ability to infect, host genotypes vary in susceptibility, and infection outcome is frequently the result of both parties' genotypic identities. These host–parasite genotype-by-genotype (GH × GP) interactions influence evolutionary and ecological dynamics in important ways. Interactions can be produced through genetic variation; however, here, we assess the role of variable gene expression as an additional source of GH × GP interactions. The bumblebee Bombus terrestris and its trypanosome gut parasite Crithidia bombi are a model system for host–parasite matching. Full-transcriptome sequencing of the bumblebee host revealed that different parasite genotypes indeed induce fundamentally different host expression responses and host genotypes vary in their responses to the infecting parasite genotype. It appears that broadly and successfully infecting parasite genotypes lead to reduced host immune gene expression relative to unexposed bees but induce the expression of genes responsible for controlling gene expression. Contrastingly, a poorly infecting parasite genotype induced the expression of immunologically important genes, including antimicrobial peptides. A targeted expression assay confirmed the transcriptome results and also revealed strong host genotype effects. In all, the expression of a number of genes depends on the host genotype and the parasite genotype and the interaction between both host and parasite genotypes. These results suggest that alongside sequence variation in coding immunological genes, variation that controls immune gene expression can also produce patterns of host–parasite specificity.
As invertebrates lack the molecular machinery employed by the vertebrate adaptive immune system, it was thought that they consequently lack the ability to produce lasting and specific immunity. ...However, in recent years, it has been demonstrated that the immune defence of invertebrates is by far more complicated and specific than previously envisioned. Lasting immunity following an initial exposure that proves protection on a secondary exposure has been shown in several species of invertebrates. This phenomenon has become known as immune priming. In the cases where it is explicitly tested, this priming can also be highly specific. In this study, we used survival assays to test for specific priming of resistance in the red flour beetle, Tribolium castaneum, using bacteria of different degrees of relatedness. Our results suggest an unexpected degree of specificity that even allows for differentiation between different strains of the same bacterium. However, our findings also demonstrate that specific priming of resistance in insects may not be ubiquitous across all bacteria.
Knowledge of the complete life cycle of a parasite is crucial to understand the epidemiology and population dynamics of a disease. The populations of several social insect pollinators are decreasing, ...and parasites are often cited as a contributing factor. The exact transmission pathway of the bumblebee parasite Crithidia bombi (Lipa & Triggiani) (Kinetoplastea: Trypanosomatidae) between two hosts is still unknown, although a previous laboratory experiment suggests transmission via the nectar of flowers. Plant species may differentially protect or negatively affect the parasite while it resides in the flower, for instance if plants vary in their floral shape or the compounds present in their nectar. This will lead to differential transmission success and potentially influence disease epidemiology. In the present study we aimed at determining whether the parasite may indeed be transmitted in the nectar by the bumblebee Bombus terrestris (L.) (Hymenoptera: Apidae). We found that parasite survival was significantly decreased in water with higher sugar concentrations. However, none of the field‐collected nectar samples contained parasite cells, and no parasite cells were transmitted between two artificial flowers by a foraging worker under laboratory conditions. Our results suggest instead that parasite cells may be deposited on flower surfaces and transported on worker surfaces.