Gut microbiota of a long‐distance migrant demonstrates resistance against environmental microbe incursions

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.     

Vertical transmission in feather mites: insights into its adaptive value

1. The consequences of symbiont transmission strategies are better understood than their adaptive causes. 2. Feather mites are permanent ectosymbionts of birds assumed to be transmitted mainly vertically from parents to offspring. The transmission of Proctophyllodes doleophyes Gaud (Astigmata, Proctophyllodidae) was studied in two European populations of pied flycatchers, Ficedula hypoleuca Pallas (Passeriformes, Muscicapidae). 3. The vertical transmission of this mite species is demonstrated here with an acaricide experiment. This study also compared (for two distant populations during 4 years) patterns in reductions in mite intensity in adult birds, from egg incubation to chick‐rearing periods, with the predictions of three hypotheses on how host survival prospects and mite intraspecific competition might drive feather mites' transmission strategy. 4. The results are in agreement with previous studies and show that feather mites transmit massively from parents to chicks. 5. The magnitude of the transmission was closer to that predicted by the hypothesis based on intraspecific competition, while a bet‐hedging strategy is also partially supported.     

Gut microbiota in wild and captive Guizhou snub‐nosed monkeys,Rhinopithecus brelichi

Many colobine species—including the endangered Guizhou snub‐nosed monkey (Rhinopithecus brelichi) are difficult to maintain in captivity and frequently exhibit gastrointestinal (GI) problems. GI problems are commonly linked to alterations in the gut microbiota, which lead us to examine the gut microbial communities of wild and captive R. brelichi. We used high‐throughput sequencing of the 16S rRNA gene to compare the gut microbiota of wild (N = 7) and captive (N = 8) R. brelichi. Wild monkeys exhibited increased gut microbial diversity based on the Chao1 but not Shannon diversity metric and greater relative abundances of bacteria in the Lachnospiraceae and Ruminococcaceae families. Microbes in these families digest complex plant materials and produce butyrate, a short chain fatty acid critical to colonocyte health. Captive monkeys had greater relative abundances of Prevotella and Bacteroides species, which degrade simple sugars and carbohydrates, like those present in fruits and cornmeal, two staples of the captive R. brelichi diet. Captive monkeys also had a greater abundance of Akkermansia species, a microbe that can thrive in the face of host malnutrition. Taken together, these findings suggest that poor health in captive R. brelichi may be linked to diet and an altered gut microbiota.     

Overview of the rules of the microbial engagement in the gut microbiome: a step towards microbiome therapeutics

Human gut microbiome is a diversified, resilient, immuno-stabilized, metabolically active and physiologically essential component of the human body. Scientific explorations have been made to seek in-depth information about human gut microbiome establishment, microbiome functioning, microbiome succession, factors influencing microbial community dynamics and the role of gut microbiome in health and diseases. Extensive investigations have proposed the microbiome therapeutics as a futuristic medicine for various physiological and metabolic disorders. A comprehensive outlook of microbial colonization, host–microbe interactions, microbial adaptation, commensal selection and immuno-survivability is still required to catalogue the essential genetic and physiological features for the commensal engagement. Evolution of a structured human gut microbiome relies on the microbial flexibility towards genetic, immunological and physiological adaptation in the human gut. Key features for commensalism could be utilized in developing tailor-made microbiome-based therapy to overcome various physiological and metabolic disorders. This review describes the key genetics and physiological traits required for host–microbe interaction and successful commensalism to institute a human gut microbiome.     

Age‐related changes in the gut microbiota of wild House Sparrow nestlings

Here, we document the development of the House Sparrow Passer domesticus gut microbiota for the benefit of future ecological and evolutionary studies in this widely used avian system. We collected and inventoried luminal and mucosal samples from the distal guts of nestling House Sparrows between 3 and 12 days of age, and also collected similar samples from adult birds. Luminal bacterial community membership and structure differed significantly between nestlings and adults. The relative abundance of Proteobacteria in the lumen decreased around day 9, whereas the relative abundance of Firmicutes increased, demonstrating age‐related changes in the microbiota of House Sparrows.     

Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Mistletoe macroecology: spatial patterns in species diversity and host use across Australia

Mistletoes are parasitic plants, the spatial distributions of which are poorly understood on macroecological scales. Because of their highly unusual life history, investigating mistletoe macroecology may provide new insight into broad‐scale patterns in species distributions. We collated data on the spatial distribution and host use of 65 species of Loranthaceous mistletoes across the continent of Australia, and tested two predictions. First, we predicted mistletoe diversity would be unrelated to productivity (i.e. evapotranspiration and precipitation), as the parasitic lifestyle might relax environmental constraints on their distributions. Second, we predicted that mistletoe host ranges (number of infected host species) would increase in areas with more potential host species. The basis of this prediction is that greater host generality is likely to evolve in regions with greater host diversity because of greater unpredictability in encounter rates with particular host species. Conversely, in regions with fewer potential hosts, randomly dispersing mistletoe propagules are likely to repeatedly encounter particular host species, thus favouring the evolution of host specialization. The results were generally consistent with these predictions. Mistletoe diversity across Australia was weakly associated with environmental conditions, whereas mistletoe host ranges increased significantly with total plant diversity. Macroecological patterns in mistletoes are unusual. In contrast to non‐parasitic plants, mistletoe diversity is poorly correlated with productivity. Host ranges varied predictably across Australia, providing the first quantitative support for the hypothesis that mistletoes in diverse regions tend to be host generalists, whereas mistletoes in depauperate regions tend to be host specialists. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 459–468.     

The effects of taxonomy,diet, and ecology on the microbiota of riverine macroinvertebrates

Freshwater macroinvertebrates play key ecological roles in riverine food webs, such as the transfer of nutrients to consumers and decomposition of organic matter. Although local habitat quality drives macroinvertebrate diversity and abundance, little is known about their microbiota. In most animals, the microbiota provides benefits, such as increasing the rate at which nutrients are metabolized, facilitating immune system development, and defending against pathogenic attack. Our objectives were to identify the bacteria within aquatic invertebrates and determine whether their composition varied with taxonomy, habitat, diet, and time of sample collection. In 2016 and 2017, we collected 264 aquatic invertebrates from the mainstem Saint John (Wolastoq) River in New Brunswick, Canada, representing 15 orders. We then amplified the V3‐V4 hypervariable region of the 16S rRNA gene within each individual, which revealed nearly 20,000 bacterial operational taxonomic units (OTUs). The microbiota across all aquatic invertebrates were dominated by Proteobacteria (69.25% of the total sequence reads), but they differed significantly in beta diversity, both among host invertebrate taxa (genus‐, family‐, and order‐levels) and temporally. In contrast to previous work, we observed no microbiota differences among functional feeding groups or traditional feeding habits, and neither water velocity nor microhabitat type structured microbiota variability. Our findings suggest that host invertebrate taxonomy was the most important factor in modulating the composition of the microbiota, likely through a combination of vertical and horizontal bacterial transmission, and evolutionary processes. This is one of the most comprehensive studies of freshwater invertebrate microbiota to date, and it underscores the need for future studies of invertebrate microbiota evolution and linkages to environmental bacteria and physico‐chemical conditions.     

Kin recognition in Drosophila: the importance of ecology and gut microbiota

The animal gut commonly contains a large reservoir of symbiotic microbes. Although these microbes have obvious functions in digestion and immune defence, gut microbes can also affect behaviour. Here, we explore whether gut microbiota has a role in kin recognition. We assessed whether relatedness, familiarity and food eaten during development altered copulation investment in three species of Drosophila with diverse ecologies. We found that a monandrous species exhibited true kin recognition, whereas familiarity determined kin recognition in a species living in dense aggregations. Finally, in a food generalist species, food eaten during development masked kin recognition. The effect of food type on copulation duration, in addition to the removal of this effect via antibiotic treatment, suggests the influence of bacteria associated with the gut. Our results provide the first evidence that varied ecologically determined mechanisms of kin recognition occur in Drosophila, and that gut bacteria are likely to have a key role in these mechanisms.     

Microbiology and immunology: An ideal partnership for a tango at the gut surface—A tribute to Philippe Sansonetti

Over the past 20 years, the highly dynamic interactions that take place between hosts and the gut microbiota have emerged as a major determinant in health and disease. The complexity of the gut microbiota represents, however, a considerable challenge, and reductionist approaches are indispensable to define the contribution of individual bacteria to host responses and to dissect molecular mechanisms. In this tribute to Philippe Sansonetti, I would like to show how rewarding collaborations with microbiologists have guided our team of immunologists in the study of host–microbiota interactions and, thanks to the use of controlled colonisation experiments in gnotobiotic mice, toward the demonstration that segmented filamentous bacteria (SFB) are indispensable to drive the post‐natal maturation of the gut immune barrier in mice. The work led with Philippe Sansonetti to set up in vitro culture conditions has been one important milestone that laid the ground for in‐depth characterization of the molecular attributes of this unusual symbiont. Recent suggestions that SFB may be present in the human microbiota encourage further cross‐fertilising interactions between microbiologists and immunologists to define whether results from mice can be translated to humans and, if so, how SFB may be used to promote human intestinal defences against enteropathogens. Nurturing the competences to pursue this inspiring project is one legacy of Philippe Sansonetti.     

Lessons from the diet: Captivity and sex shape the gut microbiota in an oviparous lizard (Calotes versicolor)

Studies have indicated that the abundance and community structure of gut microbiota are altered by diet. In this study, next‐generation sequencing of the 16S rRNA gene amplicon was performed to evaluate variations in the gut microbiota of wild and captive individuals of both sexes of Calotes versicolor. The results showed that there was a significant sex difference in microbial community structure for wild C. versicolor, Bacteroide was the dominant genus in wild females (WF), whereas Ochrobactrum was the dominant genus in wild males (WM). Acinetobacter and Hymenobacter were the dominant genera in WF, while Clostridium was the dominant genus in captive females (CF). The results indicated that differences in diet between wild and captive C. versicolor also resulted in variations in gut microbiota. Thus, it was not surprising that captivity and sex shape the gut microbiota in C. versicolor. In summary, the fundamental information presented about the gut microbiota of both sexes of wild (and captive females) C. versicolor, indicates that the artificial environments are not suitable for the wild C. versicolor.     

Haemoplasmas in wild rodents: Routes of transmission and infection dynamics

The way that some parasites and pathogens persist in the hostile environment of their host for long periods remains to be resolved. Here, longitudinal field surveys were combined with laboratory experiments to investigate the routes of transmission and infection dynamics of such a pathogen—a wild rodent haemotropic bacterium, specifically a Mycoplasma haemomuris‐like bacterium. Fleaborne transmission, direct rodent‐to‐rodent transmission and vertical transmission from fleas or rodents to their offspring were experimentally quantified, and indications were found that the main route of bacterial transmission is direct, although its rate of successful transmission is low (~20%). The bacterium's temporal dynamics was then compared in the field to that observed under a controlled infection experiment in field‐infected and laboratory‐infected rodents, and indications were found, under all conditions, that the bacterium reached its peak infection level after 25–45 days and then decreased to low bacterial loads, which persist for the rodent's lifetime. These findings suggest that the bacterium relies on persistency with low bacterial loads for long‐term coexistence with its rodent host, having both conceptual and applied implications.     

Chemical regulation of body feather microbiota in a wild bird

The microbiota has a broad range of impacts on host physiology and behaviour, pointing out the need to improve our comprehension of the drivers of host–microbiota composition. Of particular interest is whether the microbiota is acquired passively, or whether and to what extent hosts themselves shape the acquisition and maintenance of their microbiota. In birds, the uropygial gland produces oily secretions used to coat feathers that have been suggested to act as an antimicrobial defence mechanism regulating body feather microbiota. However, our comprehension of this process is still limited. In this study, we for the first time coupled high‐throughput sequencing of the microbiota of both body feathers and the direct environment (i.e., the nest) in great tits with chemical analyses of the composition of uropygial gland secretions to examine whether host chemicals have either specific effects on some bacteria or nonspecific broad‐spectrum effects on the body feather microbiota. Using a network approach investigating the patterns of co‐occurrence or co‐exclusions between chemicals and bacteria within the body feather microbiota, we found no evidence for specific promicrobial or antimicrobial effects of uropygial gland chemicals. However, we found that one group of chemicals was negatively correlated to bacterial richness on body feathers, and a higher production of these chemicals was associated with a poorer body feather bacterial richness compared to the nest microbiota. Our study provides evidence that chemicals produced by the host might function as a nonspecific broad‐spectrum antimicrobial defence mechanism limiting colonization and/or maintenance of bacteria on body feathers, providing new insight about the drivers of the host's microbiota composition in wild organisms.     

Gut microbial ecology of the Critically Endangered Fijian crested iguana (Brachylophus vitiensis): Effects of captivity status and host reintroduction on endogenous microbiomes

Animals often exhibit distinct microbial communities when maintained in captivity as compared to when in the wild. Such differentiation may be significant in headstart and reintroduction programs where individuals spend some time in captivity before release into native habitats. Using 16S rRNA gene sequencing, we (i) assessed differences in gut microbial communities between captive and wild Fijian crested iguanas (Brachylophus vitiensis) and (ii) resampled gut microbiota in captive iguanas released onto a native island to monitor microbiome restructuring in the wild. We used both cloacal swabs and fecal samples to further increase our understanding of gut microbial ecology in this IUCN Critically Endangered species. We found significant differentiation in gut microbial community composition and structure between captive and wild iguanas in both sampling schemes. Approximately two months postrelease, microbial communities in cloacal samples from formerly captive iguanas closely resembled wild counterparts. Interestingly, microbial communities in fecal samples from these individuals remained significantly distinct from wild conspecifics. Our results indicate that captive upbringings can lead to differences in microbial assemblages in headstart iguanas as compared to wild individuals even after host reintroduction into native conditions. This investigation highlights the necessity of continuous monitoring of reintroduced animals in the wild to ensure successful acclimatization and release.     

Genome‐wide association and genome partitioning reveal novel genomic regions underlying variation in gastrointestinal nematode burden in a wild bird

Identifying the genetic architecture underlying complex phenotypes is a notoriously difficult problem that often impedes progress in understanding adaptive eco‐evolutionary processes in natural populations. Host–parasite interactions are fundamentally important drivers of evolutionary processes, but a lack of understanding of the genes involved in the host's response to chronic parasite insult makes it particularly difficult to understand the mechanisms of host life history trade‐offs and the adaptive dynamics involved. Here, we examine the genetic basis of gastrointestinal nematode (Trichostrongylus tenuis) burden in 695 red grouse (Lagopus lagopus scotica) individuals genotyped at 384 genome‐wide SNPs. We first use genome‐wide association to identify individual SNPs associated with nematode burden. We then partition genome‐wide heritability to identify chromosomes with greater heritability than expected from gene content, due to harbouring a multitude of additive SNPs with individually undetectable effects. We identified five SNPs on five chromosomes that accounted for differences of up to 556 worms per bird, but together explained at best 4.9% of the phenotypic variance. These SNPs were closely linked to genes representing a range of physiological processes including the immune system, protein degradation and energy metabolism. Genome partitioning indicated genome‐wide heritability of up to 29% and three chromosomes with excess heritability of up to 4.3% (total 8.9%). These results implicate SNPs and novel genomic regions underlying nematode burden in this system and suggest that this phenotype is somewhere between being based on few large‐effect genes (oligogenic) and based on a large number of genes with small individual but large combined effects (polygenic).     

Gut microbial diversity across a contact zone for California voles: Implications for lineage divergence of hosts and mitonuclear mismatch in the assembly of the mammalian gut microbiome

Gut microbial diversity is thought to reflect the co‐evolution of microbes and their hosts as well as current host‐specific attributes such as genetic background and environmental setting. To explore interactions among these parameters, we characterized variation in gut microbiome composition of California voles (Microtus californicus) across a contact zone between two recently diverged lineages of this species. Because this contact zone contains individuals with mismatched mitochondrial‐nuclear genomes (cybrids), it provides an important opportunity to explore how different components of the genotype contribute to gut microbial diversity. Analyses of bacterial 16S rRNA sequences and joint species distribution modelling revealed that host genotypes and genetic differentiation among host populations together explained more than 50% of microbial community variation across our sampling transect. The ranked importance (most to least) of factors contributing to gut microbial diversity in our study populations were: genome‐wide population differentiation, local environmental conditions, and host genotypes. However, differences in microbial communities among vole populations (β‐diversity) did not follow patterns of lineage divergence (i.e., phylosymbiosis). Instead, among‐population variation was best explained by the spatial distribution of hosts, as expected if the environment is a primary source of gut microbial diversity (i.e., dispersal limitation hypothesis). Across the contact zone, several bacterial taxa differed in relative abundance between the two parental lineages as well as among individuals with mismatched mitochondrial and nuclear genomes. Thus, genetic divergence among host lineages and mitonuclear genomic mismatches may also contribute to microbial diversity by altering interactions between host genomes and gut microbiota (i.e., hologenome speciation hypothesis).     

常见疾病、抗生素及农药对意大利蜜蜂(Apis mellifera ligustica)肠道微生物多样性的影响研究进展

蜜蜂是对农业生产十分重要的授粉昆虫。蜜蜂肠道微生物与蜜蜂健康有密切关系,但肠道微生物也会受多种外界因素的影响。本文就蜜蜂疾病、抗生素等蜂病治疗药物、农药,以及益生菌的应用等对意大利蜜蜂工蜂肠道微生物影响的研究进行了归纳总结,并对蜜蜂与其肠道菌关系研究进行了展望。     

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.     

Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds

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.