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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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

The gut microbiome of animals, which serves important functions but can also contain potential pathogens, is to varying degrees under host genetic control. This can generate signals of phylosymbiosis, whereby gut microbiome composition matches host phylogenetic structure. However, the genetic mechanisms that generate phylosymbiosis and the scale at which they act remain unclear. Two non‐mutually exclusive hypotheses are that phylosymbiosis is driven by immunogenetic regions such as the major histocompatibility complex (MHC) controlling microbial composition, or by spatial structuring of neutral host genetic diversity via founder effects, genetic drift, or isolation by distance. Alternatively, associations between microbes and host phylogeny may be generated by their spatial autocorrelation across landscapes, rather than the direct effects of host genetics. In this study, we collected MHC, microsatellite, and gut microbiome data from separate individuals belonging to the Galápagos mockingbird species complex, which consists of four allopatrically distributed species. We applied multiple regression with distance matrices and Bayesian inference to test for correlations between average genetic and microbiome similarity across nine islands for which all three levels of data were available. Clustering of individuals by species was strongest when measured with microsatellite markers and weakest for gut microbiome distributions, with intermediate clustering of MHC allele frequencies. We found that while correlations between island‐averaged gut microbiome composition and both microsatellite and MHC dissimilarity existed across species, these relationships were greatly weakened when accounting for geographic distance. Overall, our study finds little support for large‐scale control of gut microbiome composition by neutral or adaptive genetic regions across closely related bird phylogenies, although this does not preclude the possibility that host genetics shapes gut microbiome at the individual level. [ABSTRACT FROM AUTHOR]

The host‐associated core microbiome was originally coined to refer to common groups of microbes or genes that were likely to be particularly important for host biological function. However, the term has evolved to encompass variable definitions across studies, often identifying key microbes with respect to their spatial distribution, temporal stability or ecological influence, as well as their contribution to host function and fitness.A major barrier to reaching a consensus over how to define the core microbiome and its relevance to biological, ecological and evolutionary theory is a lack of precise terminology and associated definitions, as well the persistent association of the core microbiome with host function. Common, temporal and ecological core microbiomes can together generate insights into ecological processes that act independently of host function, while functional and host‐adapted cores distinguish between facultative and near‐obligate symbionts that differ in their effects on host fitness.This commentary summarizes five broad definitions of the core microbiome that have been applied across the literature, highlighting their strengths and limitations for advancing our understanding of host–microbe systems, noting where they are likely to overlap, and discussing their potential relevance to host function and fitness.No one definition of the core microbiome is likely to capture the range of key microbes across a host population. Applied together, they have the potential to reveal different layers of microbial organization from which we can begin to understand the ecological and evolutionary processes that govern host–microbe interactions. [ABSTRACT FROM AUTHOR]

Abstract: Gut microbes are increasingly recognised for their role in regulating an animal's metabolism and immunity. However, identifying repeatable associations between host physiological processes and their gut microbiota has proved challenging, in part because microbial communities often respond stochastically to host physiological stress (e.g. fasting, forced exercise or infection). Migratory birds provide a valuable system in which to test host–microbe interactions under physiological extremes because these hosts are adapted to predictable metabolic and immunological challenges as they undergo seasonal migrations, including temporary gut atrophy during long‐distance flights. These physiological challenges may either temporarily disrupt gut microbial ecosystems, or, alternatively, promote predictable host–microbe associations during migration. To determine the relationship between migration and gut microbiota, we compared gut microbiota composition between migrating and non‐migrating (“resident”) conspecific shorebirds sharing a flock. We performed this across two sandpiper species, Calidris ferruginea and Calidris ruficollis, in north‐western Australia, and an additional C. ruficollis population 3,000 km away in southern Australia. We found that migrants consistently had higher abundances of the bacterial genus Corynebacterium (average 28% abundance) compared to conspecific residents (average <1% abundance), with this effect holding across both species and sites. However, other than this specific association, community structure and diversity was almost identical between migrants and residents, with migration status accounting for only 1% of gut community variation when excluding Corynebacterium. Our findings suggest a consistent relationship between Corynebacterium and Calidris shorebirds during migration, with further research required to identify causal mechanisms behind the association, and to elucidate functionality to the host. However, outside this specific association, migrating shorebirds broadly maintained gut community structure, which may allow them to quickly recover gut function after a migratory flight. This study provides a rare example of a repeatable and specific response of the gut microbiota to a major physiological challenge across two species and two distant populations. [ABSTRACT FROM AUTHOR]

Migratory animals are widely assumed to play an important role in the long-distance dispersal of parasites, and are frequently implicated in the global spread of zoonotic pathogens such as avian influenzas in birds and Ebola viruses in bats. However, infection imposes physiological and behavioural constraints on hosts that may act to curtail parasite dispersal via changes to migratory timing ('migratory separation') and survival ('migratory culling')., There remains little consensus regarding the frequency and extent to which migratory separation and migratory culling may operate, despite a growing recognition of the importance of these mechanisms in regulating transmission dynamics in migratory animals., We quantitatively reviewed 85 observations extracted from 41 studies to examine how both infection status and infection intensity are related to changes in body stores, refuelling rates, movement capacity, phenology and survival in migratory hosts across taxa., Overall, host infection status was weakly associated with reduced body stores, delayed migration and lower survival, and more strongly associated with reduced movement. Infection intensity was not associated with changes to host body stores, but was associated with moderate negative effects on movement, phenology and survival., In conclusion, we found evidence for negative effects of infection on host phenology and survival, but the effects were relatively small. This may have implications for the extent to which migratory separation and migratory culling act to limit parasite dispersal in migratory systems. We propose a number of recommendations for future research that will further advance our understanding of how migratory separation and migratory culling may shape host-parasite dynamics along migratory routes globally. [ABSTRACT FROM AUTHOR]

Migratory animals encounter suites of novel microbes as they move between disparate sites during their migrations, and are frequently implicated in the global spread of pathogens. Although wild animals have been shown to source a proportion of their gut microbiota from their environment, the susceptibility of migrants to enteric infections may be dependent upon the capacity of their gut microbiota to resist incorporating encountered microbes. To evaluate migrants' susceptibility to microbial invasion, we determined the extent of microbial sourcing from the foraging environment and examined how this influenced gut microbiota dynamics over time and space in a migratory shorebird, the Red-necked stint Calidris ruficollis. Contrary to previous studies on wild, nonmigratory hosts, we found that stint on their nonbreeding grounds obtained very little of their microbiota from their environment, with most individuals sourcing only 0.1% of gut microbes from foraging sediment. This microbial resistance was reflected at the population level by only weak compositional differences between stint flocks occupying ecologically distinct sites, and by our finding that stint that had recently migrated 10,000 km did not differ in diversity or taxonomy from those that had inhabited the same site for a full year. However, recent migrants had much greater abundances of the genus Corynebacterium, suggesting a potential microbial response to either migration or exposure to a novel environment. We conclude that the gut microbiota of stint is largely resistant to invasion from ingested microbes and that this may have implications for their susceptibility to enteric infections during migration. [ABSTRACT FROM AUTHOR]

Highly pathogenic avian influenza (HPAI) H5Nx viruses of the goose/Guangdong/96 lineage continue to cause outbreaks in poultry and wild birds globally. Shorebirds, known reservoirs of avian influenza viruses, migrate from Siberia to Australia along the East-Asian-Australasian Flyway. We examined whether migrating shorebirds spending nonbreeding seasons in Australia were exposed to HPAI H5 viruses. We compared those findings with those for a resident duck species. We screened >1,500 blood samples for nucleoprotein antibodies and tested positive samples for specific antibodies against 7 HPAI H5 virus antigens and 2 low pathogenicity avian influenza H5 virus antigens. We demonstrated the presence of hemagglutinin inhibitory antibodies against HPAI H5 virus clade 2.3.4.4 in the red-necked stint (Calidris ruficolis). We did not find hemagglutinin inhibitory antibodies in resident Pacific black ducks (Anas superciliosa). Our study highlights the potential role of long-distance migratory shorebirds in intercontinental spread of HPAI H5 viruses. [ABSTRACT FROM AUTHOR]

Daily light–dark cycles shape the circadian physiology and behaviour of nearly all organisms, with variation in circadian phenotypes having cascading effects on individual fitness, species interactions and species co‐evolution.Recent evidence that circadian rhythms in host immunity and metabolism are synchronised by the gut microbiota suggest that the circadian dynamics of gut microbes are a crucial component of their function. However, there remains little knowledge or understanding of the diurnal dynamics of gut microbiomes in natural populations or the consequences for host physiology and ecology.Here, we summarise the hallmarks of gut microbiota oscillations reported to date and the mechanisms by which they synchronise rhythms in host immunity and metabolism. We outline the consequences for diverse biological processes such as host pathogen susceptibility and seasonal switches in metabolism, and discuss how the breakdown of these circadian interactions, for example during senescence or because of light pollution, may affect wildlife infection risk and disease.We also provide practical guidelines for the measurement of microbial oscillations in wildlife, highlighting that whilst faecal samples of wild animals are rarely available over a 24‐h period, characterising even parts of the gut microbial cycle can be informative.An improved understanding of how gut microbial diurnal rhythms manifest in wildlife is essential to fully comprehend their role in shaping variation in host circadian phenotypes and the consequences for host physiology and ecology. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]

Individual hosts differ extensively in their competence for parasites, but traditional research has discounted this variation, partly because modeling such heterogeneity is difficult. This discounting has diminished as tools have improved and recognition has grown that some hosts, the extremely competent, can have exceptional impacts on disease dynamics. Most prominent among these hosts are the superspreaders, but other forms of extreme competence (EC) exist and others await discovery; each with potentially strong but distinct implications for disease emergence and spread. Here, we propose a framework for the study and discovery of EC, suitable for different host–parasite systems, which we hope enhances our understanding of how parasites circulate and evolve in host communities. Highlights A few members of host populations, so-called superspreaders, have disproportionate impacts on the risk of infectious disease emergence and spread. Several other forms of EC exist; some of which might be exceptionally protective. To discover and understand forms of EC, it is imperative to describe the distribution of, and covariation among, traits of individual hosts that mediate the many stages of host–parasite interactions. Here, we provide a framework to do so, emphasizing how interplay among host traits related to parasite exposure behavior, susceptibility, replicability of parasites on/in hosts, and transmissibility, comprise host competence. We hope this framework helps reveal new forms of EC and informs and improves management of disease risk. [ABSTRACT FROM AUTHOR]

Data from location logging tags have revolutionised our understanding of migration ecology, but methods of tagging that do not compromise survival need to be identified. We compared resighting rates for 156 geolocator-tagged and 316 colour ringed-only whinchats on their African wintering grounds after migration to and from eastern Europe in two separate years. We experimentally varied both light stalk length (0, 5 and 10 mm) and harness material (elastic or non-elastic nylon braid tied on, leg-loop 'Rappole' harnesses) in the second year using a reasonably balanced design (all tags in the first year used an elastic harness and 10 mm light stalk). Tags weighed 0.63 g (0.01 SE), representing 4.1% of average body mass. There was no overall significant reduction in between-year resighting rate (our proxy for survival) comparing tagged and untagged birds in either year. When comparing within tagged birds, however, using a tied harness significantly reduced resighting rate by 53% on average compared to using an elastic harness (in all models), but stalk length effects were not statistically significant in any model considered. There was no strong evidence that the fit (relative tightness) or added tag mass affected survival, although tied tags were fitted more tightly later in the study, and birds fitted with tied tags later may have had lower survival. Overall, on a precautionary principle, deploying tags with non-elastic tied harnesses should be avoided because the necessary fit, so as not to reduce survival, is time-consuming to achieve and does not necessarily improve with experience. Geolocator tags of the recommended percentage of body mass fitted with elastic leg-loop harnesses and with short light stalks can be used without survival effects in small long-distance migrant birds. [ABSTRACT FROM AUTHOR]