Host-pathogen and host-microbe interactions in migratory animals and their implications for pathogen dispersal

This thesis investigated host-microbe interactions in migratory animals to examine the mechanisms by which migrants may disperse pathogens long distances. Overall, this thesis found that migratory animals do not appear to have strong capacity to pick up and disperse pathogen

Applying the core microbiome to understand host–microbe systems

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

Diurnal oscillations in gut bacterial load and composition eclipse seasonal and lifetime dynamics in wild meerkats

Circadian rhythms in gut microbiota composition are crucial for metabolic function, yet the extent to which they govern microbial dynamics compared to seasonal and lifetime processes remains unknown. Here, we investigate gut bacterial dynamics in wild meerkats (Suricata suricatta) over a 20-year period to compare diurnal, seasonal, and lifetime processes in concert, applying ratios of absolute abundance. We found that diurnal oscillations in bacterial load and composition eclipsed seasonal and lifetime dynamics. Diurnal oscillations were characterised by a peak in Clostridium abundance at dawn, were associated with temperature-constrained foraging schedules, and did not decay with age. Some genera exhibited seasonal fluctuations, whilst others developed with age, although we found little support for microbial senescence in very old meerkats. Strong microbial circadian rhythms in this species may reflect the extreme daily temperature fluctuations typical of arid-zone climates. Our findings demonstrate that accounting for circadian rhythms is essential for future gut microbiome research

Diurnal oscillations in gut bacterial load and composition eclipse seasonal and lifetime dynamics in wild meerkats.

Circadian rhythms in gut microbiota composition are crucial for metabolic function, yet the extent to which they govern microbial dynamics compared to seasonal and lifetime processes remains unknown. Here, we investigate gut bacterial dynamics in wild meerkats (Suricata suricatta) over a 20-year period to compare diurnal, seasonal, and lifetime processes in concert, applying ratios of absolute abundance. We found that diurnal oscillations in bacterial load and composition eclipsed seasonal and lifetime dynamics. Diurnal oscillations were characterised by a peak in Clostridium abundance at dawn, were associated with temperature-constrained foraging schedules, and did not decay with age. Some genera exhibited seasonal fluctuations, whilst others developed with age, although we found little support for microbial senescence in very old meerkats. Strong microbial circadian rhythms in this species may reflect the extreme daily temperature fluctuations typical of arid-zone climates. Our findings demonstrate that accounting for circadian rhythms is essential for future gut microbiome research

An experimental evaluation of the effects of geolocator design and attachment method on between-year survival on Whinchats Saxicola rubetra

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.PostprintPeer reviewe

Agricultural Fast Food: Bats Feeding in Banana Monocultures Are Heavier but Have Less Diverse Gut Microbiota

Habitat alteration for agriculture can negatively affect wildlife physiology and health by decreasing diet diversity and increasing exposure to agrochemicals for animals foraging in altered landscapes. Such negative effects may be mediated by the disruption of the gut microbiota (termed dysbiosis), yet evidence for associations between habitat alteration, wildlife health, and the gut microbiota remains scarce. We examine the association between management intensity of banana plantations and both the body condition and gut microbiota composition of nectar-feeding bats Glossophaga soricina, which commonly forage within banana plantations across Latin America. We captured and measured 196 bats across conventional monocultures, organic plantations, and natural forests in Costa Rica, and quantified gut microbiome bacterial phylogenetic diversity using 16S rRNA amplicon sequencing. We found that gut microbiota from bats foraging in conventional monocultures were overall less phylogenetically diverse than those from bats foraging in organic plantations or natural forests, both of which were characterized by diverse bacterial assemblages and individualized microbiota. Despite lower diversity, co-occurrence network complexity was higher in conventional monocultures, potentially indicating altered microbial interactions in agricultural landscapes. Bats from both organic and conventional plantations tended to be larger and heavier than their forest counterparts, reflecting the higher food supply. Overall, our study reveals that whilst both conventional monocultures and organic plantations provide a reliable food source for bats, conventional monocultures are associated with less diverse and potentially dysbiotic microbiota, whilst organic plantations promote diverse and individualized gut microbiota akin to their natural forest-foraging counterparts. Whilst the long-term negative effects of anthropogenically-altered microbiota are unclear, our study provides further evidence from a novel perspective that organic agricultural practices are beneficial for wildlife health

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

Phylogeny- and Abundance-Based Metrics Allow for the Consistent Comparison of Core Gut Microbiome Diversity Indices Across Host Species

The filtering of gut microbial datasets to retain high prevalence taxa is often performed to identify a common core gut microbiome that may be important for host biological functions. However, prevalence thresholds used to identify a common core are highly variable, and it remains unclear how they affect diversity estimates and whether insights stemming from core microbiomes are comparable across studies. We hypothesized that if macroecological patterns in gut microbiome prevalence and abundance are similar across host species, then we would expect that increasing prevalence thresholds would yield similar changes to alpha diversity and beta dissimilarity scores across host species datasets. We analyzed eight gut microbiome datasets based on 16S rRNA gene amplicon sequencing and collected from different host species to (1) compare macroecological patterns across datasets, including amplicon sequence variant (ASV) detection rate with sequencing depth and sample size, occupancy-abundance curves, and rank-abundance curves; (2) test whether increasing prevalence thresholds generate universal or host-species specific effects on alpha and beta diversity scores; and (3) test whether diversity scores from prevalence-filtered core communities correlate with unfiltered data. We found that gut microbiomes collected from diverse hosts demonstrated similar ASV detection rates with sequencing depth, yet required different sample sizes to sufficiently capture rare ASVs across the host population. This suggests that sample size rather than sequencing depth tends to limit the ability of studies to detect rare ASVs across the host population. Despite differences in the distribution and detection of rare ASVs, microbiomes exhibited similar occupancy-abundance and rank-abundance curves. Consequently, increasing prevalence thresholds generated remarkably similar trends in standardized alpha diversity and beta dissimilarity across species datasets until high thresholds above 70%. At this point, diversity scores tended to become unpredictable for some diversity measures. Moreover, high prevalence thresholds tended to generate diversity scores that correlated poorly with the original unfiltered data. Overall, we recommend that high prevalence thresholds over 70% are avoided, and promote the use of diversity measures that account for phylogeny and abundance (Balance-weighted phylogenetic diversity and Weighted Unifrac for alpha and beta diversity, respectively), because we show that these measures are insensitive to prevalence filtering and therefore allow for the consistent comparison of core gut microbiomes across studies without the need for prevalence filtering

Circadian rhythms of hosts and their gut microbiomes: Implications for animal physiology and ecology

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

Spring migration strategies of Whinchat Saxicola rubetra when successfully crossing potential barriers of the Sahara and the Mediterranean Sea

This work was supported by Chris Goodwin, A.P. Leventis Conservation Foundation, AP Leventis Ornithological Research Institute, the British Ornithologists’ Union and the Linnean Society.The flexibility for migrant land birds to be able to travel long distances rapidly without stop-overs, and thus to cross wide inhospitable areas such as deserts and oceans, is likely to be a major determinant of their survival during migration. We measured variation in flight distance, speed, and duration of major stop-overs (more than two days), using geolocator tracks of 35 Whinchats Saxicola rubetra that migrated successfully from central Nigeria to Eastern Europe in spring, and how these measures changed, or depended on age, when crossing the barriers of the Sahara or the Mediterranean Sea. Thirty-one percent of Whinchats crossed at least the Sahara and the Mediterranean before a major stop-over; 17% travelled over 4,751 km on average without any major stop-overs. Flight distance and speed during, and duration of major stop-overs after, crossing the Mediterranean Sea were indistinguishable from migration over Continental Europe. Speed during a migration leg was lowest crossing Continental Europe and fastest, with longer duration major stop-overs afterwards, when crossing the Sahara, but there was much individual variation, and start date of migration was also a good predictor of stop-over duration. As the distance travelled during a leg increased, so major stop-over duration afterwards increased (1 day for every 1000km), but the speed of travel during the leg had no effect. There were no differences in any migration characteristics with age, other than an earlier start date for adult birds. The results suggest that adaptive shortening or even dropping of daily stop-overs may occur often, allowing rapid, long-distance migration at the cost of major stop-overs afterwards, but such behaviour is not restricted to or always found when crossing barriers, even for birds on their first spring migration. The results may highlight the importance of stop-over sites rather than barrier width as the likely key component to successful migration. Individual variation in spring migration may indicate that small passerine migrants like Whinchats may be resilient to future changes in the extent of barriers they encounter, although this may not be true of first autumn migrations or if stop-over sites are lost.PostprintPeer reviewe