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Virologists. You might know a couple of them, but unless you are a virologist yourself, the probability that you have collaborated with one in the past is low. The community is relatively small, but they pack a heavy punch and are expected to play a leading role in the research into pathogens that lies ahead. You may ask why we think virologists are our future. Suffice it to say that it is not just because they have invented technologies that belong to the space age, including use of viruses as vehicles to shuttle genes into cells[1], organic nanoparticles with specific tools attached to their surfaces to get inside target cells[2], and using genetically modified viruses as therapies to fight against cancer[3]. Did you know that virologists currently only know of about 3,200 viral species but that more than 320,000 mammal-associated viruses[4] are thought to await discovery? Just think about the viruses hidden in the Arctic ice[5] or in the insects and other animals from once cut-off regions in the world, which now face ever-increasing human exposure[6]. But a heroic (as well as an apocalyptic) role for virologists may also be on the horizon, as the adoption of phage therapy may, in the future, be used to control harmful bacteria when antibiotics fail
The bipartite interactions between insect hosts and their bacterial gut microbiota, or their bacterial pathogens, are empirically and theoretically well-explored. However, direct, and indirect tripartite interactions will also likely occur inside a host. These interactions will almost certainly affect the trajectory of pathogen virulence evolution, an area that is currently under researched. The interactions within tripartite associations can be competitive, that is, exploitative-competition, interference-competition or apparent-competition. Competitive interactions will be significantly influenced by non-competitive effects, for example, immunopathology, immunosuppression, and microbiota-mediated tolerance. Considering a combination of these interactions and effects, will enable an increased understanding of the evolution of pathogen virulence. This new perspective allows us to identify several novel research questions, which we hope will be a useful framework for future research.
The soil-feeding habit is an evolutionary novelty found in some advanced groups of termites. The study of such groups is important to revealing interesting adaptations to this way-of-life. The genus Verrucositermes is one such example, characterized by peculiar outgrowths on the head capsule, antennae and maxillary palps, which are not found in any other termite. These structures have been hypothesized to be linked to the presence of a new exocrine organ, the rostral gland, whose structure has remained unexplored.
We have thus studied the ultrastructure of the epidermal layer of the head capsule of Verrucositermes tuberosus soldiers.We describe the ultrastructure of the rostral gland, which consists of class 3 secretory cells only. The dominant secretory organelles comprise rough endoplasmic reticulum and Golgi apparatus, which provide secretions delivered to the surface of the head, likely made of peptide-derived components of unclear function. We discuss a possible role of the rostral gland of soldiers as an adaptation to the frequent encounter with soil pathogens during search for new food resources.
The termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.
A broad suite of immune adaptations have evolved in social insects which hold close parallels with the immune systems of multicellular individuals. However, comparatively little is known about the evolutionary origins of immunity in social insects. We tackle this by identifying immune genes from 18 cockroach and termite species, spanning a gradient of social lifestyles. Termites have undergone contractions of major immune gene families during the early origin of the group, particularly in antimicrobial effector and receptor proteins, followed by later re-expansions in some lineages. In a comparative gene expression analysis, we find that reproductive individuals of a termite invest more in innate immune regulation than other castes. When colonies encounter immune-challenged nestmates, gene expression responses are weak in reproductives but this pattern is reversed when colony members are immune-challenged individually, with reproductives eliciting a greater response to treatment than other castes. Finally, responses to immune challenge were more comprehensive in both subsocial and solitary cockroaches compared to termites, indicating a reduced overall ability to respond to infection in termites. Our study indicates that the emergence of termite sociality was associated with the evolution of a tapered yet caste-adapted immune system.
The termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.
Social insects employ a range of behaviours to protect their colonies against disease, but little is known about how such collective behaviours are orchestrated. This is especially true for the social Blattodea (termites). We developed an experimental approach that allowed us to explore how the social response to disease is co-ordinated by multistep host-pathogen interactions. We infected the eastern subterranean termite Reticulitermes flavipes with the entomopathogenic fungus Metarhizium anisopliae, and then, at different stages of infection, reintroduced them to healthy nestmates and recorded behavioural responses. As expected, termites groomed pathogen-exposed individuals significantly more than controls; however, grooming was significantly elevated after fungal germination than before, demonstrating the importance of fungal status to hygienic behaviour. Significantly, we found that cannibalism became prevalent only after exposed termites became visibly ill, highlighting the importance of host condition as a cue for social hygienic behaviour. Our study reveals the presence of a coordinated social response to disease that depends on stage of infection. Specifically, we show how the host may play a key role in triggering its own sacrifice. Sacrificial self-flagging has been observed in other social insects: our results demonstrate that termites have independently evolved to both recognize and destructively respond to sickness.
The importance of soldiers to termite Society defence has long been recognized, but the contribution of soldiers to other societal functions, such as colony immunity, is less well understood.
We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behaviour, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection.
We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of Proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
Most of our knowledge on insect cuticular hydrocarbons (CHCs) stems from analytical techniques based on gas-chromatography coupled with mass spectrometry (GC-MS). However, this method has its limits under standard conditions, particularly in detecting compounds beyond a chain length of around C40. Here, we compare the CHC chain length range detectable by GC-MS with the range assessed by silver-assisted laser desorption/ionization mass spectrometry (Ag-LDI-MS), a novel and rarely applied technique on insect CHCs, in seven species of the order Blattodea. For all tested species, we unveiled a considerable range of very long-chain CHCs up to C58, which are not detectable by standard GC-MS technology. This indicates that general studies on insect CHCs May frequently miss compounds in this range, and we encourage future studies to implement analytical techniques extending the conventionally accessed chain length range. Furthermore, we incorporate 3D scanned insect body surface areas as an additional factor for the comparative quantification of extracted CHC amounts between our study species. CHC quantity distributions differed considerably when adjusted for body surface areas as opposed to directly assessing extracted CHC amounts, suggesting that a more accurate evaluation of relative CHC quantities can be achieved by taking body surface areas into account.
Social immune behaviors are described in a great variety of insect societies and their role in preventing emerging infectious diseases has become a major topic in insect research. The social immune system consists of multiple layers, ranging from the synthesis of external immune molecules to the coordination of individual behaviors into sophisticated collective defensive tasks. But our understanding of how complex group-level behavioral defenses are orchestrated has remained limited. We sought to address this gap in knowledge by investigating the relationship between the external activity of an important immune effector molecule in termites, Gram negative binding protein 2 (GNBP-2) and collective grooming and cannibalism. We reasoned that as an external enzyme capable of degrading entomopathogenic fungi, GNBP-2 can facilitate the spread of pathogenic molecules in the colony, and thus serve to trigger collective defenses in a manner analogous to pathogen-associated molecular signatures (PAMPs) of the individual immune system. To test whether GNBP-2 could play a role in regulating social immune behavior, we experimentally inhibited its fungicidal activity using the glycomimetic molecule, D-d-gluconolactone (GDL) and recorded collective behavioral responses to an infected nestmate. Contrary to expectations, GNBP-2 inhibition did not influence the rate or intensity of grooming of either control or fungus-infected
nestmates. By contrast, we found that the probability of being harmed through defensive cannibalistic behaviors was significantly reduced by the inhibition of GNBP-2. Our findings indicate that the regulation of collective immune behaviors may depend in part on the external secretion of an enzyme originating from the individual immune system, but that other cues are also necessary.
Social insects nesting in soil environments are in constant contact with entomopathogens and have evolved disease resistance mechanisms within a colony to prevent the occurrence and spread of infectious diseases. Among these mechanisms: mutual grooming reduces the cuticular load of pathogens, and burial of cadavers and cannibalism can prevent pathogens from replicating within the group. We explored how the rate and type of collective behavioural response is determined by stepwise infection dynamics operating at the level of the individual. Specifically, we infected the eastern subterranean termite Reticulitermes flavipes with different types of infectious particle and infection route of the entomopathogenic fungus Metarhizium anisopliae and recorded behavioural responses of nestmates to individuals at different times during the progression of infections. As expected, termites groomed conidia-exposed individuals significantly more than controls. Interestingly, grooming was significantly elevated after fungal germination than before, suggesting that pathogen growth cues act as strong stimulators of allogrooming. Conidia-exposed termites were cannibalized, but only after they became visibly ill. By contrast, termites did not groom blastospore-injected individuals more than controls at any time-point following infection. Instead, we found that blastospore-injected individuals were continually cannibalized at a low-level following injection with either viable or heat-killed blastospores, with a marked increase in cannibalism after termites injected with viable blastospores became visibly ill and were close to death. Together, these findings point to the importance of host condition as a cue for social hygienic behavior, and that the host itself appears to emit essential sickness cues that act as targets for its own sacrifice. This demonstrates that termites have independently evolved to both identify and destructively respond to sickness.
Honeybee symbionts, predominantly bacteria, play important roles in honeybee health, nutrition, and pathogen protection, thereby supporting colony health. On the other hand, fungi are often considered indicators of poor bee health, and honeybee microbiome studies generally exclude fungi and yeasts. We hypothesized that yeasts may be an important aspect of early honeybee biology, and if yeasts provide a mutual benefit to their hosts, then honeybees could provide a refuge during metamorphosis to ensure the presence of yeasts at emergence. We surveyed for yeast and fungi during pupal development and metamorphosis in worker bees using fungal-specific quantitative polymerase chain reaction (qPCR), next-generation sequencing, and standard microbiological culturing. On the basis of yeast presence in three distinct apiaries and multiple developmental stages, we conclude that yeasts can survive through metamorphosis and in naïve worker bees, albeit at relatively low levels. In comparison, known bacterial mutualists, like Gilliamella and Snodgrassella, were generally not found in pre-eclosed adult bees. Whether yeasts are actively retained as an important part of the bee microbiota or are passively propagating in the colony remains unknown. Our demonstration of the constancy of yeasts throughout development provides a framework to further understand the honeybee microbiota.
Wood-destroying pests such as Anobium punctatum and Xestobium rufovillosum cause damage to art and cultural objects as well as to buildings. Monitoring population dynamics of pest species as well as of their naturally occurring counterparts are an essential part in the development of biological control measures as alternatives to conventional wood protection. Therefore, both the dispersal and homogeneity of pest and beneficial insect populations across multiple sites and buildings were investigated in the present study using DNA barcoding. Specifically, beetles of Anobium punctatum (de Geer 1774) (Coleoptera, Ptinidae), Xestobium rufovillosum (de Geer, 1974) (Coloeptera, Ptinidae), and Korynetes caeruleus (de Geer 1775) (Coleoptera, Cleridae) were collected from buildings at four different sites in Mecklenburg-Western Pomerania, North-Eastern Germany. DNA analysis was performed using mitochondrial cytochrome c oxidase subunit I (COI). For A. punctatum, low base pair variability was found in the gene segment studied (4-5 SNPs) within one building (Greven) and between four spatially separated sites. Conversely, in X. rufovillosum, the sequences from two sites studied were homogeneous within a site but differed between locations by nine base pair positions (SNPs). The main result of this study is that the pests A. punctatum and X. rufovillosum showed a higher variability in the investigated gene segment than the natural counterpart K. caeruleus.
Results suggest a reduction in immune gene repertoires in termites and possible complementary expression between termite castes. With comparative genomics we will investigate the evolution of gene families related to immunity, try to understand where reductions and expansions take place and relate these changes to shifts in sociality and ecology. The role of TEs in expansions and contractions of immune gene families will be investigated. For these analyses, we propose to generate high quality, highly contiguous genomes of species from different levels of sociality, covering all major termite families. With comparative transcriptomics we will investigate the expression of immune genes in different castes. Via network analyses we will identify pathways indicated in differential immunity between castes and between species of different sociality levels. We will investigate how these pathways have been rewired along the transitions to higher levels of sociality and how, intra-specifically, they change between castes.
Evolution relies on the availability of genetic diversity for fitness-based selection. However, most deoxyribonucleic acid (DNA) viruses employ DNA polymerases (Pol) capable of exonucleolytic proofreading to limit mutation rates during DNA replication. The relative genetic stability produced by high-fidelity genome replication can make studying DNA virus adaptation and evolution an intensive endeavor, especially in slowly replicating viruses. Here, we present a proofreading-impaired Pol mutant (Y547S) of Marek’s disease virus that exhibits a hypermutator phenotype while maintaining unimpaired growth in vitro and wild-type (WT)-like pathogenicity in vivo. At the same time, mutation frequencies observed in Y547S virus populations are 2–5-fold higher compared to the parental WT virus. We find that Y547S adapts faster to growth in originally non-permissive cells, evades pressure conferred by antiviral inhibitors more efficiently, and is more easily attenuated by serial passage in cultured cells compared to WT. Our results suggest that hypermutator viruses can serve as a tool to accelerate evolutionary processes and help identify key genetic changes required for adaptation to novel host cells and resistance to antiviral therapy. Similarly, the rapid attenuation achieved through adaptation of hypermutators to growth in cell culture enables identification of genetic changes underlying attenuation and virulence, knowledge that could practically exploited, e.g. in the rational design of vaccines.
Wild bees are important pollinators for agricultural crops and solitary species such as Osmia bicornis are particularly suitable for pollination management. Wild bees share floral resources with managed honey bees and may be exposed to emerging infectious diseases. Although studies have explored the prevalence of pathogens in solitary wild bee species, data regarding the impact of pathogens on solitary bee health are lacking.
We carried out experiments examining whether the solitary bee species O. bicornis is susceptible to infection with the emerging pathogen The results obtained indicate that N. ceranae may be able to infect O. bicornis but its impact on host fitness is negligible: survival rates did not differ between Control and inoculated bees, although male survival was marginally lower after infection. To explore the possible field-relevance of our findings, we collected wild bees near an infected and a non-infected hive and showed that N. ceranae was shared between managed and wild bees, although only the in presence of infected honey bees.
The findings of the present study show that O. bicornis is susceptible to pathogen spillover and could act as a potential reservoir host for N. ceranae in pollinator networks. Additional studies on this species incorporating sublethal effects, multiple infections and other interacting stressors are warranted.
Wild bees are important pollinators of wild plants and agricultural crops and they are threatened by several environmental stressors including emerging pathogens. Honey bees have been suggested as a potential source of pathogen spillover. One prevalent pathogen that has recently emerged as a honey bee disease is the microsporidian Nosema ceranae. While the impacts of N. ceranae in honey bees are well documented, virtually nothing is known about its effects in solitary wild bees.
The solitary mason bee Osmia bicornis is a common pollinator in orchards and amenable to Commercial management. Here, we experimentally exposed larvae of O. bicornis to food contaminated with N. ceranae and document spore presence during larval development. We measured mortality, growth parameters, and timing of pupation in a semi-field experiment. Hatched individuals were assessed for physiological state including fat body mass, wing muscle mass, and body size. We recorded higher mortality in the viable-spore-exposed group but could only detect a low number of Spores among the individuals of this treatment. Viable-spore-treated individuals with higher head capsule width had a delayed pupation start. No impact on the physiological status could be detected in hatched imagines. Although we did not find overt evidence of O. bicornis infection, our findings indicate that exposure of larvae to viable N. ceranae spores could affect bee development.
Our understanding of RNA viruses from edible insects is minimal at best, with studies largely focusing on model insect species and those associated with obvious signs of disease. This represents a considerable gap in understanding, given the growing role of insects as a source of food and feed, as well as the more general relevance of insects in agriculture and health. Illness due to entomophagy is rare but well documented, including fatal cases following the consumption of termites. Termites are eaten commonly in tropical Asia, Africa and South America, and are among the insects with the highest recorded fat content. There are many species of termites, with a wide range of diets and habitats centering around the consumption of wood and soil substrates. In this study, we report the results from a survey of more than 30 cockroach and termite transcriptomes, with the aim of understanding the diversity and evolution of RNA viruses as well as other potentially pathogenic organisms that are associated with this relevant but somewhat overlooked group of insects. We discuss our results in the context of the possible zoonotic risk posed by insects, as well as in the context of emerging viral and other disease threats that may face insects being reared at industrial scales.
Bee populations have declined significantly in recent years and this is thought to be attributable at least in part to the (re-)emergence of viruses. These viruses are predominantly positive single stranded (+ss) RNA viruses belonging to the Picornavirales. Managed honeybees are often infested with the invasive mite, Varroa destructor, which vectors RNA viruses including Deformed wing virus (DWV, family Iflaviridae): a leading culprit of colony losses. Many bee viruses have been sequenced and structural features are now available for viruses such as DWV. DWV consists of at least 3 distinct genotypes, two of which have been shown to be differentially virulent in honeybees. Molecular studies have demonstrated that DWV has a mean evolutionary rate of 1.35 x 10-3 per site per year. For such viruses – in contrast to their eukaryotic hosts – ecological and evolutionary timescales significantly overlap. This rapid evolution allows RNA viruses to adapt quickly to novel host environments with recombination representing an additional key source of genetic variation. Interestingly, recombination between genotypes of DWV has recently been shown to be a common occurrence in honeybees. A challenge has been to develop bioinformatics tools that can accurately reconstruct viral haplotypes – including recombinants – from heterogenous high-throughput sequence data.
The impact of blood-to-blood Varroa destructor transmission on virus evolution represents an important question in bee virus research. Due to the nature of the V. destructor life cycle, predictions can be made about the potential impact of the mite on virus virulence evolution. Specifically, the developing honeybee host pupa should remain alive until close to the completion of metamorphosis to provide sufficient time for successful mite reproduction, including offspring mating. For optimal transmission, any virus found in a mature and mated daughter mite will hold a significant selective advantage over a virus found in an immature or unmated daughter mite – placing a cost on virus virulence that impacts honeybee pupae before mites can mate. On the other side, viruses replicating too slowly and with delayed virulence effects will hold a selective handicap because fewer transmission units will be found in mated mites. I have hypothesized that the evolution of virus virulence shifted following the arrival of V. destructor, with viruses, including recombinants and/or specific viral genotypes being selected for a level of virulence in pupae (and likely also in adults) that maximises R0, which represents the basic reproductive number of the virus in the host population. R0 is defined by the number of subsequent infections caused by a single infection and it must be greater than 1 for an infection to spread in a population. It is enhanced by maximising the number of transmission units passed to uninfected susceptible vectors, and ultimately hosts (Figure 1).
Honeybee viruses are also shared with sympatric wild bees and viral prevalence and sequence data indicate frequent virus transmission between managed and wild bee species. In addition to infecting the western honeybee (Apis mellifera), DWV can infect other Asian honeybee species such as Apis ceranae. Outside of honeybees, DWV has been found widely in bumblebees, including solitary bees and wasps and there is evidence that it can actively replicate in several Bombus and solitary bee species. Whether the arrival of the V. destructor mite in A. mellifera has driven viral emergence in non-Apis bees is a target of ongoing research.
Termitidae comprises 80% of all termite species that play dominant decomposer roles in Tropical cosystems. Two major events during Termite evolution were the loss of cellulolytic gut protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in ‘‘combs’’ constructed within the nest. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae, which cultivates bacterial symbionts on combs inside its nests. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae.
This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like ‘‘external rumen’’ involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized.
Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon.