Immunogenetics, sylvatic plague and its vectors: insights from the pathogen reservoir Mastomys natalensis in Tanzania.

Yersinia pestis is a historically important vector-borne pathogen causing plague in humans and other mammals. Contemporary zoonotic infections with Y. pestis still occur in sub-Saharan Africa, including Tanzania and Madagascar, but receive relatively little attention. Thus, the role of wildlife reservoirs in maintaining sylvatic plague and spillover risks to humans is largely unknown. The multimammate rodent Mastomys natalensis is the most abundant and widespread rodent in peri-domestic areas in Tanzania, where it plays a major role as a Y. pestis reservoir in endemic foci. Yet, how M. natalensis' immunogenetics contributes to the maintenance of plague has not been investigated to date. Here, we surveyed wild M. natalensis for Y. pestis vectors, i.e., fleas, and tested for the presence of antibodies against Y. pestis using enzyme-linked immunosorbent assays (ELISA) in areas known to be endemic or without previous records of Y. pestis in Tanzania. We characterized the allelic and functional (i.e., supertype) diversity of the major histocompatibility complex (MHC class II) of M. natalensis and investigated links to Y. pestis vectors and infections. We detected antibodies against Y. pestis in rodents inhabiting both endemic areas and areas considered non-endemic. Of the 111 nucleotide MHC alleles, only DRB*016 was associated with an increased infestation with the flea Xenopsylla. Surprisingly, we found no link between MHC alleles or supertypes and antibodies of Y. pestis. Our findings hint, however, at local adaptations towards Y. pestis vectors, an observation that more exhaustive sampling could unwind in the future.

MHC class II genes mediate susceptibility and resistance to coronavirus infections in bats.

Understanding the immunogenetic basis of coronavirus (CoV) susceptibility in major pathogen reservoirs, such as bats, is central to inferring their zoonotic potential. Members of the cryptic Hipposideros bat species complex differ in CoV susceptibility, but the underlying mechanisms remain unclear. The genes of the major histocompatibility complex (MHC) are the best understood genetic basis of pathogen resistance, and differences in MHC diversity are one possible reason for asymmetrical infection patterns among closely related species. Here, we aimed to link asymmetries in observed CoV (CoV-229E, CoV-2B and CoV-2Bbasal) susceptibility to immunogenetic differences amongst four Hipposideros bat species. From the 2072 bats assigned to their respective species using the mtDNA cytochrome b gene, members of the most numerous and ubiquitous species, Hipposideros caffer D, were most infected with CoV-229E and SARS-related CoV-2B. Using a subset of 569 bats, we determined that much of the existent allelic and functional (i.e. supertype) MHC DRB class II diversity originated from common ancestry. One MHC supertype shared amongst all species, ST12, was consistently linked to susceptibility with CoV-229E, which is closely related to the common cold agent HCoV-229E, and infected bats and those carrying ST12 had a lower body condition. The same MHC supertype was connected to resistance to CoV-2B, and bats with ST12 were less likely be co-infected with CoV-229E and CoV-2B. Our work suggests a role of immunogenetics in determining CoV susceptibility in bats. We advocate for the preservation of functional genetic and species diversity in reservoirs as a means of mitigating the risk of disease spillover.

Climate change drives loss of bacterial gut mutualists at the expense of host survival in wild meerkats.

Climate change and climate-driven increases in infectious disease threaten wildlife populations globally. Gut microbial responses are predicted to either buffer or exacerbate the negative impacts of these twin pressures on host populations. However, examples that document how gut microbial communities respond to long-term shifts in climate and associated disease risk, and the consequences for host survival, are rare. Over the past two decades, wild meerkats inhabiting the Kalahari have experienced rapidly rising temperatures, which is linked to the spread of tuberculosis (TB). We show that over the same period, the faecal microbiota of this population has become enriched in Bacteroidia and impoverished in lactic acid bacteria (LAB), a group of bacteria including Lactococcus and Lactobacillus that are considered gut mutualists. These shifts occurred within individuals yet were compounded over generations, and were better explained by mean maximum temperatures than mean rainfall over the previous year. Enriched Bacteroidia were additionally associated with TB exposure and disease, the dry season and poorer body condition, factors that were all directly linked to reduced future survival. Lastly, abundances of LAB taxa were independently and positively linked to future survival, while enriched taxa did not predict survival. Together, these results point towards extreme temperatures driving an expansion of a disease-associated pathobiome and loss of beneficial taxa. Our study provides the first evidence from a longitudinally sampled population that climate change is restructuring wildlife gut microbiota, and that these changes may amplify the negative impacts of climate change through the loss of gut mutualists. While the plastic response of host-associated microbiotas is key for host adaptation under normal environmental fluctuations, extreme temperature increases might lead to a breakdown of coevolved host-mutualist relationships.

Co-infections mask pathogen-specific associations with the gut microbiota in wild voles.

Research Highlight: Brila, I., Lavirinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T. & Watts, P. C. (2022). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole (Myodes glareolus). Journal of Animal Ecology, https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.13869. Interactions between pathogens and host-associated microbial communities can influence host fitness, disease progression and pathogen emergence. The vast majority of studies characterize interactions between single pathogens and bacterial commensals, yet co-infections with multiple pathogens are the norm in nature. In their paper on pathogen-microbiome interactions, Brila et al. (2022) examine how co-infections with four systemic pathogens associate with the gut microbiota in wild bank voles. Building on a series of tests, the authors show that excluding co-infection information from statistical models masks pathogen-specific patterns and confounds interpretations. This paper advances on previous studies by generating surveillance data on a phylogenetically diverse suite of vole pathogens to address the question as to whether pathogens exhibit unique or universal associations with gut commensals. They report that even bacterial pathogens with similar transmission ecology have divergent associations with gut microbes, and highlight that a mechanistic understanding of host-pathogen interactions is necessary for decoding the diverse consequences for gut microbial communities.

Gut microbiota individuality is contingent on temporal scale and age in wild meerkats.

Inter-individual differences in gut microbiota composition are hypothesized to generate variation in host fitness-a premise for the evolution of host-gut microbe symbioses. However, recent evidence suggests that gut microbial communities are highly dynamic, challenging the notion that individuals harbour unique gut microbial phenotypes. Leveraging a long-term dataset of wild meerkats, we reconcile these concepts by demonstrating that the relative importance of identity for shaping gut microbiota phenotypes depends on the temporal scale. Across meerkat lifespan, year-to-year variation overshadowed the effects of identity and social group in predicting gut microbiota composition, with identity explaining on average less than 2% of variation. However, identity was the strongest predictor of microbial phenotypes over short sampling intervals (less than two months), predicting on average 20% of variation. The effect of identity was also dependent on meerkat age, with the gut microbiota becoming more individualized and stable as meerkats aged. Nevertheless, while the predictive power of identity was negligible after two months, gut microbiota composition remained weakly individualized compared to that of other meerkats for up to 1 year. These findings illuminate the degree to which individualized gut microbial signatures can be expected, with important implications for the time frames over which gut microbial phenotypes may mediate host physiology, behaviour and fitness in natural populations.

Interaction between MHC diversity and constitution, gut microbiota and Astrovirus infections in a neotropical bat.

Astroviruses (AstVs) infect numerous mammalian species including reservoirs such as bats. Peptides encoded by the genes of the highly polymorphic Major Histocompatibility Complex (MHC) form the first line of host defence against pathogens. Aside from direct involvement in mounting adaptive immune responses, MHC class II genes are hypothesized to regulate gut commensal diversity and shape the production of immune-modulatory substances by microbes, indirectly affecting host susceptibility. Despite initial empirical evidence for the link between host MHC and the microbiota, associations among these factors remain largely unknown. To fill this gap, we examined MHC allelic diversity and constitution, the gut bacterial community and abundance pattern of a wild population of a neotropical bat (Artibeus jamaicensis) challenged by AstV infections. First, we show an age-dependent relationship between the host MHC class II diversity and constitution and the gut microbiota in AstV-uninfected bats. Crucially, these associations changed in AstV-infected bats. Additionally, we identify changes in the abundance of specific bacterial taxa linked to the presence of certain MHC supertypes and AstV infection. We suggest changes in the microbiota to be either a result of AstV infection or the MHC-mediated modulation of microbial communities. The latter could subsequently affect microbe-mediated immunity and resistance against AstV infection. Our results emphasize that the reciprocal nature of host immune genetics, gut microbial diversity and pathogen infection require attention, which are particularly important given their repercussions for disease susceptibility and severity in wild animal populations with a history of zoonotic spillover and frequent human contact.

Rapid Divergence of Predator Functional Traits Affects Prey Composition in Aquatic Communities.

Identifying traits that underlie variation in individual performance of consumers (i.e., trait utility) can help reveal the ecological causes of population divergence and the subsequent consequences for species interactions and community structure. Here, we document a case of rapid divergence (over the past 100 generations, or ∼150 years) in foraging traits and feeding efficiency between a lake and stream population pair of threespine stickleback. Building on predictions from functional trait models of fish feeding, we analyzed foraging experiments with a Bayesian path analysis and elucidated the traits explaining variation in foraging performance and the species composition of ingested prey. Despite extensive previous research on the divergence of foraging traits among populations and ecotypes of stickleback, our results provide novel experimental evidence of trait utility for jaw protrusion, gill raker length, and gill raker spacing when foraging on a natural zooplankton assemblage. Furthermore, we discuss how these traits might contribute to the differential effects of lake and stream stickleback on their prey communities, observed in both laboratory and mesocosm conditions. More generally, our results illustrate how the rapid divergence of functional foraging traits of consumers can impact the biomass, species composition, and trophic structure of prey communities.

Two decades of tuberculosis surveillance reveal disease spread, high levels of exposure and mortality and marked variation in disease progression in wild meerkats.

Infections with tuberculosis (TB)-causing agents of the Mycobacterium tuberculosis complex threaten human, livestock and wildlife health globally due to the high capacity to cross trans-species boundaries. Tuberculosis is a cryptic disease characterized by prolonged, sometimes lifelong subclinical infections, complicating disease monitoring. Consequently, our understanding of infection risk, disease progression, and mortality across species affected by TB remains limited. The TB agent Mycobacterium suricattae was first recorded in the late 1990s in a wild population of meerkats inhabiting the Kalahari in South Africa and has since spread considerably, becoming a common cause of meerkat mortality. This offers an opportunity to document the epidemiology of naturally spreading TB in a wild population. Here, we synthesize more than 25 years' worth of TB reporting and social interaction data across 3420 individuals to track disease spread, and quantify rates of TB social exposure, progression, and mortality. We found that most meerkats had been exposed to the pathogen within eight years of first detection in the study area, with exposure reaching up to 95% of the population. Approximately one quarter of exposed individuals progressed to clinical TB stages, followed by physical deterioration and death within a few months. Since emergence, 11.6% of deaths were attributed to TB, although the true toll of TB-related mortality is likely higher. Lastly, we observed marked variation in disease progression among individuals, suggesting inter-individual differences in both TB susceptibility and resistance. Our results highlight that TB prevalence and mortality could be higher than previously reported, particularly in species or populations with complex social group dynamics. Long-term studies, such as the present one, allow us to assess temporal variation in disease prevalence and progression and quantify exposure, which is rarely measured in wildlife. Long-term studies are highly valuable tools to explore disease emergence and ecology and study host-pathogen co-evolutionary dynamics in general, and its impact on social mammals.

A framework for testing the impact of co-infections on host gut microbiomes.

Parasitic infections disturb gut microbial communities beyond their natural range of variation, possibly leading to dysbiosis. Yet it remains underappreciated that most infections are accompanied by one or more co-infections and their collective impact is largely unexplored. Here we developed a framework illustrating changes to the host gut microbiome following single infections, and build on it by describing the neutral, synergistic or antagonistic impacts on microbial α- and ß-diversity expected from co-infections. We tested the framework on microbiome data from a non-human primate population co-infected with helminths and Adenovirus, and matched patterns reported in published studies to the introduced framework. In this case study, α-diversity of co-infected Malagasy mouse lemurs (Microcebus griseorufus) did not differ in comparison with that of singly infected or uninfected individuals, even though community composition captured with ß-diversity metrices changed significantly. Explicitly, we record stochastic changes in dispersion, a sign of dysbiosis, following the Anna-Karenina principle rather than deterministic shifts in the microbial gut community. From the literature review and our case study, neutral and synergistic impacts emerged as common outcomes from co-infections, wherein both shifts and dispersion of microbial communities following co-infections were often more severe than after a single infection alone, but microbial α-diversity was not universally altered. Important functions of the microbiome may also suffer from such heavily altered, though no less species-rich microbial community. Lastly, we pose the hypothesis that the reshuffling of host-associated microbial communities due to the impact of various, often coinciding parasitic infections may become a source of novel or zoonotic diseases.

Noise pollution on coral reefs? - A yet underestimated threat to coral reef communities.

Noise pollution is an anthropogenic stressor that is increasingly recognized for its negative impact on the physiology, behavior and fitness of marine organisms. Driven by the recent expansion of maritime shipping, artisanal fishing and tourism (e.g., motorboats used for recreational purpose), underwater noise increased greatly on coral reefs. In this review, we first provide an overview on how reef organisms sense and use sound. Thereafter we review the current knowledge on how underwater noise affects different reef organisms. Although the majority of available examples are limited to few fish species, we emphasize how the impact of noise differs based on an organisms' acoustic sensitivity, mobility and developmental stage, as well as between noise type, source and duration. Finally, we highlight measures available to governments, the shipping industry and individual users and provide directions for polices and research aimed to manage this global issue of noise emission on coral reefs.

Transgenerational selection driven by divergent ecological impacts of hybridizing lineages.

Dynamic interactions between ecological conditions and the phenotypic composition of populations likely play an important role in evolution, but the direction and strength of these feedbacks remain difficult to characterize. We investigated these dynamics across two generations of threespine sticklebacks from two evolutionary lineages undergoing secondary contact and hybridization. Independently manipulating the density and lineage of adults in experimental mesocosms led to contrasting ecosystem conditions with strong effects on total survival in a subsequent generation of juveniles. Ecosystem modifications by adults also varied the strength of selection on competing hybrid and non-hybrid juveniles. This variation in selection indicated (1) a negative eco-evolutionary feedback driven by lineage-specific resource depletion and dependence and (2) a large performance advantage of hybrid juveniles in depleted environments. This work illustrates the importance of interactions between phenotype, population density and the environment in shaping selection and evolutionary trajectories, especially in the context of range expansion with secondary contact and hybridization.

Successful therapy for a patient with an infected ascending aortic graft and sternal osteomyelitis without graft removal.

OBJECTIVE: Following open-heart surgery, sternal osteomyelitis or infection of the graft may be a serious complication with high mortality rates. The recommended treatment of an infected graft is its explantation. Because of the poor performance status of the patient, this may not always be an option. We report a successful treatment concept without removal of the infected graft. METHODS: The infected ascending aortic graft and the remaining sternum of a critically ill 60-year-old man were covered with a bilateral pectoralis muscle flap. RESULTS: Postoperatively, the laboratory test values normalized and the patient was discharged 1 month after the intervention. One year after surgery, the patient was in good condition and the examination showed no signs of infection. CONCLUSION: The thus demonstrated treatment concept with insertion of well-vascularized tissues in combination with a specific antibiotic regime in our hands proved to be an additional option for the successful management of life-threatening infections of a sternal osteomyelitis in combination of an infected aortic graft.

Posterior auricular perichondrial cutaneous graft combined with cartilage strip in nostril reconstruction.

OBJECTIVE: Reconstruction of alar structures of the nose remains difficult. The result has to be not only functional but also aesthetic. Different solutions to reconstruct alar defects are feasible. A good result that meets the specific demands on stability, aesthetics, and stable architecture without shrinkage of the area is not easily achieved. METHOD: A perichondrial cutaneous graft (PCCG), a graft consisting of a perichondral layer, fatty tissue, and skin that is harvested retroauriculary, is combined with an attached cartilage strip. CASE RESULT: A 72-year-old patient suffering from basal cell carcinoma of the ala of the nose underwent the reconstructive procedure with a good result in 1 year in terms of stability, color match, and graft take. CONCLUSION: First, a strip of cartilage had been included in a PCCG where tumor resection required sacrifice of more than 50% of the alar rim. The case shows that one can consider a cartilage strip-enhanced PCCG graft to reconstruct alar defects.