Host Behavior Research Articles

Microbiota's Role in Diet-Driven Alterations in Food Intake: Satiety, Energy Balance, and Reward.

The gut microbiota plays a key role in modulating host physiology and behavior, particularly feeding behavior and energy homeostasis. There is accumulating evidence demonstrating a role for gut microbiota in the etiology of obesity. In human and rodent studies, obesity and high-energy feeding are most consistently found to be associated with decreased bacterial diversity, changes in main phyla relative abundances and increased presence of pro-inflammatory products. Diet-associated alterations in microbiome composition are linked with weight gain, adiposity, and changes in ingestive behavior. There are multiple pathways through which the microbiome influences food intake. This review discusses these pathways, including peripheral mechanisms such as the regulation of gut satiety peptide release and alterations in leptin and cholecystokinin signaling along the vagus nerve, as well as central mechanisms, such as the modulation of hypothalamic neuroinflammation and alterations in reward signaling. Most research currently focuses on determining the role of the microbiome in the development of obesity and using microbiome manipulation to prevent diet-induced increase in food intake. More studies are necessary to determine whether microbiome manipulation after prolonged energy-dense diet exposure and obesity can reduce intake and promote meaningful weight loss.

The Influence of Habitat on Viral Diversity in Neotropical Rodent Hosts.

Rodents are important reservoirs of numerous viruses, some of which have significant impacts on public health. Ecosystem disturbances and decreased host species richness have been associated with the emergence of zoonotic diseases. In this study, we aimed at (a) characterizing the viral diversity in seven neotropical rodent species living in four types of habitats and (b) exploring how the extent of environmental disturbance influences this diversity. Through a metagenomic approach, we identified 77,767 viral sequences from spleen, kidney, and serum samples. These viral sequences were attributed to 27 viral families known to infect vertebrates, invertebrates, plants, and amoeba. Viral diversities were greater in pristine habitats compared with disturbed ones, and lowest in peri-urban areas. High viral richness was observed in savannah areas. Differences in these diversities were explained by rare viruses that were generally more frequent in pristine forest and savannah habitats. Moreover, changes in the ecology and behavior of rodent hosts, in a given habitat, such as modifications to the diet in disturbed vs. pristine forests, are major determinants of viral composition. Lastly, the phylogenetic relationships of four vertebrate-related viral families (Polyomaviridae, Flaviviridae, Togaviridae, and Phenuiviridae) highlighted the wide diversity of these viral families, and in some cases, a potential risk of transmission to humans. All these findings provide significant insights into the diversity of rodent viruses in Amazonia, and emphasize that habitats and the host’s dietary ecology may drive viral diversity. Linking viral richness and abundance to the ecology of their hosts and their responses to habitat disturbance could be the starting point for a better understanding of viral emergence and for future management of ecosystems.

Cross Talk between Viruses and Insect Cells Cytoskeleton.

Viruses are excellent manipulators of host cellular machinery, behavior, and life cycle, with the host cell cytoskeleton being a primordial viral target. Viruses infecting insects generally enter host cells through clathrin-mediated endocytosis or membrane fusion mechanisms followed by transport of the viral particles to the corresponding replication sites. After viral replication, the viral progeny egresses toward adjacent cells and reaches the different target tissues. Throughout all these steps, actin and tubulin re-arrangements are driven by viruses. The mechanisms used by viruses to manipulate the insect host cytoskeleton are well documented in the case of alphabaculoviruses infecting Lepidoptera hosts and plant viruses infecting Hemiptera vectors, but they are not well studied in case of other insect–virus systems such as arboviruses–mosquito vectors. Here, we summarize the available knowledge on how viruses manipulate the insect host cell cytoskeleton, and we emphasize the primordial role of cytoskeleton components in insect virus motility and the need to expand the study of this interaction.

Drivers of change and stability in the gut microbiota of an omnivorous avian migrant exposed to artificial food supplementation.

Human activities shape resources available to wild animals, impacting diet and probably altering their microbiota and overall health. We examined drivers shaping microbiota profiles of common cranes (Grus grus) in agricultural habitats by comparing gut microbiota and crane movement patterns (GPS-tracking) over three periods of their migratory cycle, and by analysing the effect of artificially supplemented food provided as part of a crane-agriculture management programme. We sampled faecal droppings in Russia (nonsupplemented, premigration) and in Israel in late autumn (nonsupplemented, postmigration) and winter (supplemented and nonsupplemented, wintering). As supplemented food is typically homogenous, we predicted lower microbiota diversity and different composition in birds relying on supplementary feeding. We did not observe changes in microbial diversity with food supplementation, as diversity differed only in samples from nonsupplemented wintering sites. However, both food supplementation and season affected bacterial community composition and led to increased abundance of specific genera (mostly Firmicutes). Cranes from the nonsupplemented groups spent most of their time in agricultural fields, probably feeding on residual grain when available, while food-supplemented cranes spent most of their time at the feeding station. Thus, nonsupplemented and food-supplemented diets probably diverge only in winter, when crop rotation and depletion of anthropogenic resources may lead to a more variable diet in nonsupplemented sites. Our results support the role of diet in structuring bacterial communities and show that they undergo both seasonal and human-induced shifts. Movement analyses provide important clues regarding host diet and behaviour towards understanding how human-induced changes shape the gut microbiota in wild animals.

The Repressor C Protein, Pf4r, Controls Superinfection of Pseudomonas aeruginosa PAO1 by the Pf4 Filamentous Phage and Regulates Host Gene Expression.

It has been shown that the filamentous phage, Pf4, plays an important role in biofilm development, stress tolerance, genetic variant formation and virulence in Pseudomonas aeruginosa PAO1. These behaviours are linked to the appearance of superinfective phage variants. Here, we have investigated the molecular mechanism of superinfection as well as how the Pf4 phage can control host gene expression to modulate host behaviours. Pf4 exists as a prophage in PAO1 and encodes a homologue of the P2 phage repressor C and was recently named Pf4r. Through a combination of molecular techniques, ChIPseq and transcriptomic analyses, we show a critical site in repressor C (Pf4r) where a mutation in the site, 788799A>G (Ser4Pro), causes Pf4r to lose its function as the immunity factor against reinfection by Pf4. X-ray crystal structure analysis shows that Pf4r forms symmetric homo-dimers homologous to the E.coli bacteriophage P2 RepC protein. A mutation, Pf4r*, associated with the superinfective Pf4r variant, found at the dimer interface, suggests dimer formation may be disrupted, which derepresses phage replication. This is supported by multi-angle light scattering (MALS) analysis, where the Pf4r* protein only forms monomers. The loss of dimerisation also explains the loss of Pf4r’s immunity function. Phenotypic assays showed that Pf4r increased LasB activity and was also associated with a slight increase in the percentage of morphotypic variants. ChIPseq and transcriptomic analyses suggest that Pf4r also likely functions as a transcriptional regulator for other host genes. Collectively, these data suggest the mechanism by which filamentous phages play such an important role in P. aeruginosa biofilm development.

Nestling behaviour predicts naris deformation in Darwin’s finches parasitized by the avian vampire fly

Abstract Although in-nest parasitism can reduce the fitness of avian hosts, the severity of these effects may vary with host physiology and behaviour. If certain nestling behaviours are beneficial for resisting parasitism, then selection may favour some behavioural phenotypes over others. Here, we tested whether differences in nestling behaviour mediate the negative effects of parasitism, using small ground finches (Geospiza fuliginosa), on Floreana Island, that had been parasitized by the invasive avian vampire fly (Philornis downsi). We first established, using 4 years of breeding data (2005, 2006, 2010 and 2020), that nestlings exposed to more parasites had larger nares and, among older nestlings only, lower body mass. We then examined, using data from the 2020 season, whether each nestling’s behaviour (specifically, its response to human handling) predicted the severity of its naris deformation. When faced with high-intensity parasitism, more responsive nestlings (i.e. those that struggled more during handling) had larger nares compared to more docile nestlings. This suggests that more responsive nestlings suffer greater fitness costs due to parasitism, although we also discuss alternative explanations. Future work should consider the stability and heritability of these nestling behavioural differences and whether parasite-induced selection shapes behavioural variation at the population level.

Evolution of human respiratory virus epidemics.

Background: Pathogens are often assumed to evolve towards reduced virulence, but counterexamples abound. Faced with a new pathogen, such as SARS-CoV-2, it is crucial to be able to forecast the case fatality rate (CFR) and the overall disease burden. Considerable effort has been invested towards developing a mathematical framework for predicting virulence evolution. Although many approaches accurately recapitulate complex outcomes, most rely on an assumed trade-off between CFR and infection rate. It is often impractical to empirically validate this constraint for human pathogens. Methods: A compartment model with parameters tuning the degree to which symptomatic individuals are isolated and the duration of immunity is constructed and evaluated at both short timescales and at equilibrium. Results: We reveal kinetic constraints whereby variation of multiple parameters in concert leads to decreased CFR and increased pathogen fitness, whereas independent variation of the parameters decreases pathogen fitness. Smallpox, SARS-CoV-2, and influenza are analyzed as diverse representatives of human respiratory viruses. We show that highly virulent viruses, such as smallpox, are often constrained by the host behavior, whereas moderately virulent viruses, such as SARS-CoV-2, appear to be typically constrained by the relationship between the duration of immunity and CFR. Conclusions: Evolution of human respiratory epidemics appears to be often kinetically constrained and a reduction in CFR should not be assumed. These results agree with previous work demonstrating an increase in virulence for smallpox and further predict that SARS-CoV-2 is likely to continue presenting a substantial disease burden. Herd immunity against SARS-CoV-2 and viruses with similar life history traits might be unachievable without vaccination. However, partial isolation of symptomatic individuals can have a major effect on the epidemic dynamics not only by reducing the number of fatalities in the short term but also by changing the evolutionary trajectory of moderate CFR viruses towards reduced CFR.

Assessing age, breeding stage, and mating activity as drivers of variation in the reproductive microbiome of female tree swallows.

Sexually transmitted microbes are hypothesized to influence the evolution of reproductive strategies. Though frequently discussed in this context, our understanding of the reproductive microbiome is quite nascent. Indeed, testing this hypothesis first requires establishing a baseline understanding of the temporal dynamics of the reproductive microbiome and of how individual variation in reproductive behavior and age influence the assembly and maintenance of the reproductive microbiome as a whole. Here, we ask how mating activity, breeding stage, and age influence the reproductive microbiome. We use observational and experimental approaches to explain variation in the cloacal microbiome of free‐living, female tree swallows (Tachycineta bicolor). Using microsatellite‐based parentage analyses, we determined the number of sires per brood (a proxy for female mating activity). We experimentally increased female sexual activity by administering exogenous 17ß‐estradiol. Lastly, we used bacterial 16S rRNA amplicon sequencing to characterize the cloacal microbiome. Neither the number of sires per brood nor the increased sexual activity of females significantly influenced female cloacal microbiome richness or community structure. Female age, however, was positively correlated with cloacal microbiome richness and influenced overall community structure. A hypothesis to explain these patterns is that the effect of sexual activity and the number of mates on variation in the cloacal microbiome manifests over an individual's lifetime. Additionally, we found that cloacal microbiome alpha diversity (Shannon Index, Faith's phylogenetic distance) decreased and community structure shifted between breeding stages. This is one of few studies to document within‐individual changes and age‐related differences in the cloacal microbiome across successive breeding stages. More broadly, our results contribute to our understanding of the role that host life history and behavior play in shaping the cloacal microbiomes of wild birds.

Invasion history shapes host transcriptomic response to a body-snatching parasite.

By shuffling biogeographical distributions, biological invasions can both disrupt long-standing associations between hosts and parasites and establish new ones. This creates natural experiments with which to study the ecology and evolution of host-parasite interactions. In estuaries of the Gulf of Mexico, the white-fingered mud crab (Rhithropanopeus harrisii) is infected by a native parasitic barnacle, Loxothylacus panopaei (Rhizocephala), which manipulates host physiology and behaviour. In the 1960s, L.panopaei was introduced to the Chesapeake Bay and has since expanded along the southeastern Atlantic coast, while host populations in the northeast have so far been spared. We use this system to test the host's transcriptomic response to parasitic infection and investigate how this response varies with the parasite's invasion history, comparing populations representing (i) long-term sympatry between host and parasite, (ii) new associations where the parasite has invaded during the last 60years and (iii) naïve hosts without prior exposure. A comparison of parasitized and control crabs revealed a core response, with widespread downregulation of transcripts involved in immunity and moulting. The transcriptional response differed between hosts from the parasite's native range and where it is absent, consistent with previous observations of increased susceptibility in populations lacking exposure to the parasite. Crabs from the parasite's introduced range, where prevalence is highest, displayed the most dissimilar response, possibly reflecting immune priming. These results provide molecular evidence for parasitic manipulation of host phenotype and the role of gene regulation in mediating host-parasite interactions.

Evolution of human respiratory virus epidemics

Background: Pathogens are often assumed to evolve towards reduced virulence, but counterexamples abound. Faced with a new pathogen, such as SARS-CoV-2, it is crucial to be able to forecast the case fatality rate (CFR) and the overall disease burden. Considerable effort has been invested towards developing a mathematical framework for predicting virulence evolution. Although many approaches accurately recapitulate complex outcomes, most rely on an assumed trade-off between CFR and infection rate. It is often impractical to empirically validate this constraint for human pathogens.Methods: A compartment model with parameters tuning the degree to which symptomatic individuals are isolated and the duration of immunity is constructed and evaluated at both short timescales and at equilibrium.Results: We reveal kinetic constraints whereby variation of multiple parameters in concert leads to decreased CFR and increased pathogen fitness, whereas independent variation of the parameters decreases pathogen fitness. Smallpox, SARS-CoV-2, and influenza are analyzed as diverse representatives of human respiratory viruses. We show that highly virulent viruses, such as smallpox, are often constrained by the host behavior, whereas moderately virulent viruses, such as SARS-CoV-2, appear to be typically constrained by the relationship between the duration of immunity and CFR.Conclusions: Evolution of human respiratory epidemics appears to be often kinetically constrained and a reduction in CFR should not be assumed. These results agree with previous work demonstrating an increase in virulence for smallpox and further predict that SARS-CoV-2 is likely to continue presenting a substantial disease burden. Herd immunity against SARS-CoV-2 and viruses with similar life history traits might be unachievable without vaccination. However, partial isolation of symptomatic individuals can have a major effect on the epidemic dynamics not only by reducing the number of fatalities in the short term but also by changing the evolutionary trajectory of moderate CFR viruses towards reduced CFR.

Understanding potential implications for non-trophic parasite transmission based on vertebrate behavior at mesocarnivore carcass sites

High infection risk is often associated with aggregations of animals around attractive resources. Here, we explore the behavior of potential hosts of non-trophically transmitted parasites at mesocarnivore carcass sites. We used videos recorded by camera traps at 56 red fox (Vulpes vulpes) carcasses and 10 carcasses of other wild carnivore species in three areas of southeastern Spain. Scavenging species, especially wild canids, mustelids and viverrids, showed more frequent rubbing behavior at carcass sites than non-scavenging and domestic species, suggesting that they could be exposed to a higher potential infection risk. The red fox was the species that most frequently contacted carcasses and marked and rubbed carcass sites. Foxes contacted heterospecific carcasses more frequently and earlier than conspecific ones and, when close contact occurred, it was more likely to be observed at heterospecific carcasses. This suggests that foxes avoid contact with the type of carcass and time period that have the greatest risk as a source of parasites. Overall, non-trophic behaviors of higher infection risk were mainly associated with visitor-carcass contact and visitor contact with feces and urine, rather than direct contact between visitors. Moreover, contact events between scavengers and carnivore carcasses were far more frequent than consumption events, which suggests that scavenger behavior is more constrained by the risk of acquiring meat-borne parasites than non-trophically transmitted parasites. This study contributes to filling key gaps in understanding the role of carrion in the landscape of disgust, which may be especially relevant in the current global context of emerging and re-emerging pathogens.Graphical abstract

Migration and tolerance shape host behaviour and response to parasite infection.

Numerous theoretical models have demonstrated that migration, a seasonal animal movement behaviour, can minimize the risks and costs of parasite infection. Past work on migration-infection interactions assumes migration is the only strategy available to organisms for dealing with the parasite infection, that is they migrate to a different environment to recover or escape from infection. Thus, migration is similar to the non-spatial strategy of resistance, where hosts prevent infection or kill parasites once infected. However, an alternative defence strategy is to tolerate the infection and experience a lower cost to the infection. To our knowledge, no studies have examined how migration can change based on combining two host strategies (migration and tolerance) for dealing with parasites. In this paper, we aim to understand how both parasite transmission and infection tolerance can influence the host's migratory behaviour. We constructed a model that incorporates two host strategies (migration and tolerance) to understand whether allowing for tolerance affects the proportion of the population that migrates at equilibrium in response to infection. We show that the benefits of tolerance can either decrease or increase the host's migration. Also, if the benefit of migration is great, then individuals are more likely to migrate regardless of the presence of tolerance. Finally, we find that the transmission rate of parasite infection can either decrease or increase the tolerant host's migration, depending on the cost of migration. These findings highlight that adopting two defence strategies is not always beneficial to the hosts. Instead, a single strategy is often better, depending on the costs and benefits of the strategies and infection pressures. Our work further suggests that multiple host-defence strategies as a potential explanation for the evolution of migration to minimize the parasite infection. Moreover, migration can also affect the ecological and evolutionary dynamics of parasite-host interactions.

Toxoplasma gondii infections are associated with costly boldness toward felids in a wild host

Toxoplasma gondii is hypothesized to manipulate the behavior of warm-blooded hosts to promote trophic transmission into the parasite’s definitive feline hosts. A key prediction of this hypothesis is that T. gondii infections of non-feline hosts are associated with costly behavior toward T. gondii’s definitive hosts; however, this effect has not been documented in any of the parasite’s diverse wild hosts during naturally occurring interactions with felines. Here, three decades of field observations reveal that T. gondii-infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality. We discuss these results in light of 1) the possibility that hyena boldness represents an extended phenotype of the parasite, and 2) alternative scenarios in which T. gondii has not undergone selection to manipulate behavior in host hyenas. Both cases remain plausible and have important ramifications for T. gondii’s impacts on host behavior and fitness in the wild.

Geospatial Modelling and Univariate Analysis of Commensal Rodent-Borne Cestodoses: The Case of Invasive spp. of Rattus and Indigenous Mastomys coucha From South Africa.

Poor socio-economic and unsanitary conditions are conducive to commensal rodent infestations, and these conditions are widespread in South Africa. Cestode species of zoonotic interest are highly prevalent in commensal rodents, such as invasive Rattus norvegicus, Rattus rattus, Rattus tanezumi, and indigenous Mastomys coucha, and have been frequently recovered from human stool samples. These cestode species have similar transmission dynamics to traditional soil-transmitted helminths (STHs), which ties them to infections associated with poverty and poor sanitation. Univariate analysis was used in the present study to determine the association between rodent-related factors and cestode prevalence, while ecological niche modelling was used to infer the potential distribution of the cestode species in South Africa. Cestode prevalence was found to be associated with older rodents, but it was not significantly associated with sex, and ectoparasite presence. The predicted occurrence for rodent-borne cestodes predominantly coincided with large human settlements, typically associated with significant anthropogenic changes. In addition, cestode parasite occurrence was predicted to include areas both inland and along the coast. This is possibly related to the commensal behaviour of the rodent hosts. The study highlights the rodent-related factors associated with the prevalence of parasites in the host community, as well as the environmental variables associated with parasite infective stages that influence host exposure. The application of geospatial modelling together with univariate analysis to predict and explain rodent-borne parasite prevalence may be useful to inform management strategies for targeted interventions.

Supplier-origin mouse microbiomes significantly influence locomotor and anxiety-related behavior, body morphology, and metabolism

The mouse is the most commonly used model species in biomedical research. Just as human physical and mental health are influenced by the commensal gut bacteria, mouse models of disease are influenced by the fecal microbiome (FM). The source of mice represents one of the strongest influences on the FM and can influence the phenotype of disease models. The FM influences behavior in mice leading to the hypothesis that mice of the same genetic background from different vendors, will have different behavioral phenotypes. To test this hypothesis, colonies of CD-1 mice, rederived via embryo transfer into surrogate dams from four different suppliers, were subjected to phenotyping assays assessing behavior and physiological parameters. Significant differences in behavior, growth rate, metabolism, and hematological parameters were observed. Collectively, these findings show the profound influence of supplier-origin FMs on host behavior and physiology in healthy, genetically similar, wild-type mice maintained in identical environments.

Evolution of human respiratory virus epidemics.

Background: It is often assumed that pathogens evolve towards reduced virulence, but counterexamples abound. Faced with a new pathogen, such as SARS-CoV-2, it is highly desirable to be able to forecast the case fatality rate (CFR) and overall disease burden into the future. Considerable effort has been invested towards the development of a mathematical framework for predicting virulence evolution. Although many approaches accurately recapitulate complex outcomes, most rely on an assumed trade-off between CFR and infection rate. It is often impractical to empirically validate this constraint for human pathogens. Methods: A compartment model with parameters tuning the degree to which symptomatic individuals are isolated and the duration of immunity is constructed and evaluated at both short timescales and at equilibrium (when it exists). Results: We reveal kinetic constraints where the variation of multiple parameters in concert leads to decreased CFR and increased pathogen fitness, whereas independent variation of the parameters decreases pathogen fitness. Smallpox, SARS-CoV-2, and influenza are analyzed as diverse representatives of human respiratory viruses. We show that highly virulent viruses, such as smallpox, are likely often constrained by host behavior, whereas moderately virulent viruses, such as SARS-CoV-2, appear to be typically constrained by the relationship between the duration of immunity and CFR. Conclusions: Evolution of human respiratory epidemics appears to be often kinetically constrained and a reduction in CFR should not be assumed. Our findings imply that, without continued public health intervention, SARS-CoV-2 is likely to continue presenting a substantial disease burden. The existence of a parameter regime admitting endemic equilibrium suggests that herd immunity is unachievable. However, we demonstrate that even partial isolation of symptomatic individuals can have a major effect not only by reducing the number of fatalities in the short term but also by potentially changing the evolutionary trajectory of the virus towards reduced CFR.

Neuro-Signals from Gut Microbiota: Perspectives for Brain Glioma.

Simple SummaryIn the last few years, a lot of evidence demonstrated an unexpected bidirectional communication among the gut microbes and the brain. Gut microbiota derived molecules may affect the nervous system in physiological and pathological conditions, even modulating neurotransmitter levels. Here, we summarize the effects of neurotransmitters on the proliferation and differentiation of neuronal precursor cells in the adult brain, and in brain gliomas. Further, we discuss the hypothesis that modulation of neurotransmitters by gut microbiota might impact the development and progress of brain tumor, specifically glioma. Further investigation on the mechanisms involved in the bidirectional gut-brain communication is required to identify new molecular and cellular targets involved in the dysregulation of brain homeostasis occurring in glioma.Glioblastoma (GBM) is the most aggressive form of glioma tumor in adult brain. Among the numerous factors responsible for GBM cell proliferation and invasion, neurotransmitters such as dopamine, serotonin and glutamate can play key roles. Studies performed in mice housed in germ-free (GF) conditions demonstrated the relevance of the gut-brain axis in a number of physiological and pathological conditions. The gut–brain communication is made possible by vagal/nervous and blood/lymphatic routes and pave the way for reciprocal modulation of functions. The gut microbiota produces and consumes a wide range of molecules, including neurotransmitters (dopamine, norepinephrine, serotonin, gamma-aminobutyric acid [GABA], and glutamate) that reach their cellular targets through the bloodstream. Growing evidence in animals suggests that modulation of these neurotransmitters by the microbiota impacts host neurophysiology and behavior, and affects neural cell progenitors and glial cells, along with having effects on tumor cell growth. In this review we propose a new perspective connecting neurotransmitter modulation by gut microbiota to glioma progression.

Heterospecific competitors and seasonality can affect host physiology and behavior: key factors in disease transmission

AbstractEcological and environmental factors can influence the transmission of infectious diseases. They can accomplish this via effects on host susceptibility and exposure to infection, which are governed by host physiology and behavior, respectively. To better inform disease control, more information is needed about how extrinsic factors affect physiological and behavioral processes that determine transmission. We investigated how heterospecific competitors and seasonality may influence host susceptibility and intraspecific contact rates using a directly transmitted disease system, the North American deer mouse (Peromyscus maniculatus)—Sin Nombre hantavirus (SNV) system. In grasslands of western Montana, USA, deer mice compete with dominant voles (Microtus spp.) and shrews (Sorex spp.) and experience a seasonal temperate climate. Higher SNV transmission occurs primarily during spring/summer, when changes in physiology and behavior may serve as influential contributors. We hypothesized that (1) voles, and to a lesser extent shrews, will induce chronic stress, suppress immunity, and may change contact rates of deer mice; and (2) during spring/summer, deer mice may experience chronic stress, suppressed immunity, and higher contact rates, which may help explain the reported seasonality in SNV transmission. Over two years, we trapped small mammals at four grids in western Montana. Deer mice were sampled for feces and blood and evaluated for scar numbers, demography, and body condition scores (BCSs). We evaluated stress physiology with fecal corticosterone metabolites (FCMs), neutrophil/lymphocyte (N/L) ratios and BCSs, immunity with white blood cell (WBC) counts, and contact rates with scar numbers. We found that shrew density was negatively associated with stress response FCMs, suggestive of chronic stress. Additionally, although complex interactions existed, shrew and vole densities were negatively associated with BCSs, but differentially with scar numbers. N/L ratios were higher in spring/summer, whereas WBC counts were lower in summer, suggestive of chronic stress and suppressed immunity, respectively. Our results suggest that (1) heterospecific competitors may differentially influence disease transmission via stress physiology and contact rates, and that (2) chronic stress, suppressed immunity, and higher contact rates may help explain why higher SNV transmission has been previously reported during spring/summer in Montana. Our findings may extend to other directly transmitted disease systems.

Enhanced polarotaxis can explain water-entry behaviour of mantids infected with nematomorph parasites

A wide range of parasites manipulate the behaviours of their hosts in order to complete their life cycle1. Alteration of phototaxis is thought to be involved in host manipulation in many cases2,3. However, very little is known about what features of the light (intensity, spectrum, polarization) alter behaviour. Here we report that arboreal mantids (Hierodula patellifera) infected by nematomorph parasites (Chordodes sp.) are attracted to horizontally polarized light, which could induce the mantids to enter water, where the parasites can then emerge and reproduce. In a two-choice test, infected mantids were attracted to horizontally but not vertically polarized light. Uninfected mantids were not attracted to either. In a field experiment, 14 infected mantids entered a deep pool, where the water surface strongly reflected horizontally polarized light. By contrast, only two mantids entered a shallow pool, where the surface reflection had higher light intensity but weaker polarization. To our knowledge, this is the first study demonstrating that a manipulative parasite can take advantage of its hosts' ability to perceive polarized light stimuli to alter host behaviour. VIDEO ABSTRACT.

The call of the wild: using non-model systems to investigate microbiome-behaviour relationships.

On and within most sites across an animal's body live complex communities of microorganisms. These microorganisms perform a variety of important functions for their hosts, including communicating with the brain, immune system and endocrine axes to mediate physiological processes and affect individual behaviour. Microbiome research has primarily focused on the functions of the microbiome within the gastrointestinal tract (gut microbiome) using biomedically relevant laboratory species (i.e. model organisms). These studies have identified important connections between the gut microbiome and host immune, neuroendocrine and nervous systems, as well as how these connections, in turn, influence host behaviour and health. Recently, the field has expanded beyond traditional model systems as it has become apparent that the microbiome can drive differences in behaviour and diet, play a fundamental role in host fitness and influence community-scale dynamics in wild populations. In this Review, we highlight the value of conducting hypothesis-driven research in non-model organisms and the benefits of a comparative approach that assesses patterns across different species or taxa. Using social behaviour as an intellectual framework, we review the bidirectional relationship between the gut microbiome and host behaviour, and identify understudied mechanisms by which these effects may be mediated.