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Differences in gut similarity and association networks within groups per age category, female reproductive state, and male dominance. A, C GuniFrac distances between group members of different or same age categories or rank categories of adult group members only. As there is only one dominant male per group, we could not compare two dominant individuals. We did not have enough adult female group members to compare their GuniFrac distances during different reproductive stages. B, D, E ASVs associated with the different age categories, adult female reproductive stages, or rank categories within groups, respectively. The association network was calculated and visualised in the same way as described in Fig. 1. The network for age categories only contains data from the late dry seasons 2016/2017 since animals were only considered infants, when they were < 9 months of age. Hence, during the early dry seasons, there were no infants in the population
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Background
Various aspects of sociality can benefit individuals’ health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social microbiome, the collective microbial metacommunity...
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Background
Wildlife conservation often focuses on establishing protected areas. However, these conservation zones are frequently established without adequate knowledge of the movement patterns of the species they are designed to protect. Understanding movement and foraging patterns of species in dynamic and diverse habitats can allow managers to de...
In mammals, olfactory communication plays an essential role in territorial and mating dynamics. Scent depositions in various species, including lemurs, can be placed via marking or overmarking (marking over previous depositions). We focused on the role that marking and overmarking play in territorial defence and intrasexual competition. We investig...
Citations
... However, with relatively few studies comparing lab and wild Mus musculus microbiotas to date, it remains unclear in which respects lab mouse microbiotas consistently differ from those of their wild counterparts, including in functional and phenotypic characteristics, as well as temporal stability. Considering how the gut microbiota varies across a wider range of genetic and environmental backgrounds in both lab and wild settings [14][15][16][17] is important to comprehensively understand the extent to which domestication has influenced the gut microbiota of the house mouse. Improved cataloguing of the house mouse gut microbiota across space and time is also important for developing a relevant range of natural microbiotas for use in wildreconstituted lab model organisms [18] and knowledge of which common gut microbes should be included in mouse-specific synthetic communities. ...
The mammalian gut microbiota is a complex microbial community with diverse impacts on host biology. House mice (Mus musculus) are the major model organism for research on mammals, but laboratory domestication has altered their gut microbiota from that of their wild counterparts. Knowledge about how and why the gut microbiota of this species varies between lab and wild settings and among natural populations could improve its utility as a model organism. Here, we use a large dataset comprising over 800 house mouse samples from multiple laboratory facilities and strains and wild mice from mainland and island populations to investigate gut microbiota variation in this species across contrasting genetic and environmental settings. Across geographically disparate populations, we find that wild mice possess a gut microbiota that is compositionally distinct, displays a higher relative abundance and richness of aerotolerant taxa, and is taxonomically and functionally more diverse than that of lab mice. Longitudinally sampled wild mice also display markedly higher temporal turnover in microbiota composition than lab mice. Wild mice from oceanic islands harboured microbiotas that differed subtly from those of mainland wild mice and were more divergent from lab mouse microbiotas. These findings highlight much greater spatial and temporal turnover of gut microbes in wild compared to laboratory mice.
... Due to the combined homogenizing effects of social interactions plus shared environment, diet, and genetic relatedness, populations living in sympatry tend to share more similar microbiomes (e.g., Greene et al. 2019a;Rudolph et al. 2022). An important next step in our understanding of host-microbe evolution is mapping how the microbiome diffuses across a dynamic landscape. ...
... This pattern likely arose through a combination of familial relatedness (i.e., vertical microbial transmission), shared environment and diet, and within-group social cohesion (e.g., transfer of microbiota via grooming). The importance of social group fits within a larger framework, as previous work in a congeneric species (Propithecus verreauxi) has shown that different social groups harbored distinct gut microbiomes (Rudolph et al. 2022), and that this distinction could be maintained over multiple years despite major shifts in group composition (Perofsky et al. 2021). ...
This study uses a biogeographic framework to identify patterns of gut microbiome divergence in an endangered lemur species endemic to Madagascar's southeastern rainforests, the Milne‐Edwards's sifaka ( Propithecus edwardsi) . Specifically, we tested the effects of (1) geographic barriers, (2) habitat disturbance, and (3) geographic distance on gut microbiome alpha and beta diversity. We selected 10 social groups from 4 sites in Ranomafana National Park with varied histories of selective logging. Sites were spaced between 4 and 17 km apart falling on either side of two parallel barriers to animal movement: the Namorona River and the RN25 highway. Using 16S rRNA metabarcoding, we found the greatest beta diversity differentiation to occur between social groups, with significant divisions on opposite sides of geographic barriers (road/river). Habitat disturbance had the most significant effect on alpha diversity, though, contrary to many other studies, disturbance was associated with higher microbial species richness. Without biomedical context, it is unclear whether microbiome differences observed herein are neutral, adaptive, or maladaptive. However, microbiome divergence associated with the road/river may be a symptom of reduced host gene flow, warranting further investigation and perhaps conservation action (e.g., construction of wildlife bridges). Finally, this work demonstrates that significant microbiome variation can accrue over small sampling areas, lending new insight into host‐microbe‐environmental interactions.
... First, the GM of cohabiting individuals often resembles one another. For instance, cohabiting humans (e.g., spouses) and group members in free-ranging NHPs (e.g., chimpanzees, baboons, and lemurs) exhibit greater similarity in GM composition than those not sharing a home [23,[43][44][45] or social group [19,21,41,46], respectively. Second, when individuals migrate from living together to apart (or vice versa), concomitant shifts in the microbiota follow. ...
Background
The gut microbiota (GM) has proven to be essential for both physical health and mental wellbeing, yet the forces that ultimately shape its composition remain opaque. One critical force known to affect the GM is the social environment. Prior work in humans and free-ranging non-human primates has shown that cohabitation and frequent social interaction can lead to changes in GM composition. However, it is difficult to assess the direction of causation in these studies, and interpretations are complicated by the influence of uncontrolled but correlated factors, such as shared diet.
Results
We performed a 15-month longitudinal investigation wherein we disentangled the impacts of diet and social living conditions on GM composition in a captive cohort of 13 male cynomolgus macaques. The animals were in single housing for the first 3 months of the study initially with a variable diet. After baseline data collection they were placed on a controlled diet for the remainder of the study. Following this diet shift the animals were moved to paired housing for 6 months, enabling enhanced social interaction, and then subsequently returned to single housing at the end of our study. This structured sequencing of diet and housing changes allowed us to assess their distinct impacts on GM composition. We found that the early dietary adjustments led to GM changes in both alpha and beta diversity, whereas changes in social living conditions only altered beta diversity. With respect to the latter, we found that two particular bacterial families — Lactobacillaceae and Clostridiaceae — demonstrated significant shifts in abundance during the transition from single housing to paired housing, which was distinct from the shifts we observed based on a change in diet. Conversely, we found that other bacteria previously associated with sociality were not altered based on changes in social living conditions but rather only by changes in diet.
Conclusions
Together, these findings decouple the influences that diet and social living have on GM composition and reconcile previous observations in the human and animal literatures. Moreover, the results indicate biological alterations of the gut that may, in part, mediate the relationship between sociality and wellbeing.
... The mammalian gut microbiota has diverse impacts on host biology with key roles in modulating processes ranging from metabolism to behaviour [1][2][3] . The composition and diversity of this internal ecosystem varies between individuals, populations, and species and also within individuals over time [4][5][6] . The gut microbiota matures in early life, during which marked changes in composition and diversity occur [7][8][9] . ...
Assembly of the mammalian gut microbiota during early life is known to shape key aspects of organismal development, including immunity, metabolism and behaviour. While house mice (Mus musculus) are the major laboratory model organism for gut microbiota research, their artificial lab-based lifestyle could fundamentally alter ecological processes of microbiota assembly and dynamics, in ways that affect their usefulness as a model system. To examine this, here we directly compared patterns of gut microbiota assembly in house mice from the lab and from the wild, making use of a tractable, individually-marked wild population where we could examine patterns of gut microbiota assembly during early life. Despite lab and wild mice harbouring taxonomically distinct communities, we identify striking similarities in multiple patterns of their gut microbiota assembly. Specifically, age-related changes in both alpha and beta diversity, as well as the abundance of predominant phyla and aerotolerance of the microbiota followed parallel trajectories in both settings. These results suggest some degree of intrinsic programme in gut microbiota assembly that transcends variation in taxonomic profiles, and the genetic and environmental background of the host. They further support the notion that despite their artificial environment, lab mice can provide meaningful insights into natural microbiota ecological dynamics in early life and their interplay with host development.
... Further, we only tested two pied tamarin groups. Callitrichid groups are often composed by family members (Mustoe 2023), genetic and social proximity may relate to specific physiology aspects of the digestion, or the composition of microorganisms that act during digestion (Rudolph et al. 2022). Thus, it would be desirable to replicate the experiment with other tamarin groups. ...
Frugivory and seed dispersal are fundamental ecological interactions influencing plant population dynamics and distribution. Still, understanding how the ingestion of seeds by fruit-eating animals affects seedling emergence performance remains poorly documented. Seed dispersal through animal ingestion can either promote or hinder germination. In this study, we assessed how seed ingestion by Saguinus bicolor, a critically endangered primate from the Brazilian Amazon, affects germination rate and germinability. As primate seed ingestion often improves seed germination, we predicted that germination rate and germinability would be higher in seeds defecated by the tamarins if compared to hand-extracted seeds. Of the 23 species, five did not germinated in either the control or gut-passage treatments. Among the ones that germinated, nine had an average increase in germinability, two decreased in germinability, and seven had a neutral effect. The germination rate increased in four species, reduced in eight species and had a neutral effect in six of the species. Most of the seeds that passed through the tamarins' digestive tract successfully germinated, demonstrating that seed ingestion by pied tamarins can benefit the plant populations by dispersing viable seeds through the landscape.
... However, while temporal shifts in the gut microbiome may buffer short-term environmental changes, social interactions between group members may be more important for maintaining the presence of host-associated microbes that are beneficial within a specific habitat or during a particular time of year (33,34). In this regard, group membership has been shown to more strongly predict gut micro biome composition than temporal differences in diet in certain host species (17,(35)(36)(37). For example, group membership explained 18.6% of the variation in gut microbiome composition and 10.8% of the variation in gut microbiome function in wild baboons (Papio cynocephalus) (38). ...
The gut microbiome has the potential to buffer temporal variations in resource availability and consumption, which may play a key role in the ability of animals to adapt to a broad range of habitats. We investigated the temporal composition and function of the gut microbiomes of wild common marmosets (Callithrix jacchus) exploiting a hot, dry environment—Caatinga—in northeastern Brazil. We collected fecal samples during two time periods (July–August and February–March) for 2 years from marmosets belonging to eight social groups. We used 16S rRNA gene amplicon sequencing, metagenomic sequencing, and butyrate RT-qPCR to assess changes in the composition and potential function of their gut microbiomes. Additionally, we identified the plant, invertebrate, and vertebrate components of the marmosets’ diet via DNA metabarcoding. Invertebrate, but not plant or vertebrate, consumption varied across the year. However, gut microbiome composition and potential function did not markedly vary across study periods or as a function of diet composition. Instead, the gut microbiome differed markedly in both composition and potential function across marmosets residing in different social groups. We highlight the likely role of factors, such as behavior, residence, and environmental heterogeneity, in modulating the structure of the gut microbiome.
IMPORTANCE
In a highly socially cohesive and cooperative primate, group membership more strongly predicts gut microbiome composition and function than diet.
... The overgrowth of Proteobacteria, which include numerous pathogenic genera of bacteria, has been suggested as a signature of dysbiosis and disease in humans, including metabolic disorders, inflammation, and cancer (Rizzatti et al., 2017;Shin et al., 2015). This compositional shift might reflect host or environmental changes that could lead to dysbiotic gut microbiomes or natural variations in the group such as different feeding strategies (Mallott et al., 2018), the age of the individuals (Reveles et al., 2019), reproductive state (Sun et al., 2020), or social status (Rudolph et al., 2022) for example. A comparison of the three social groups showed the presence of Actinobacteria only in individuals inhabiting Vale do Aleixo. ...
The Northern muriqui (Brachyteles hypoxanthus) is one of the world's most critically endangered primates, with only ~1000 mature individuals remaining in the wild. Habitat loss and hunting have led to its sharp decline, making conservation efforts crucial. Analyses of gut microbiomes in wild populations can provide valuable information on host health and vulnerability, and ultimately, contribute to baseline knowledge toward improving conservation programs and reintroduction efforts. In this study, we analyzed the microbiome (16S rRNA metabarcoding) of fecal samples belonging to 53 uniquely genotyped individuals from three social groups from the Caparaó National Park, aiming to provide the first assessment of the microbiome diversity and composition for this species. Our results showed the muriqui gut microbiome was predominantly composed of the phyla Bacteroidetes and Firmicutes, with the dominant classes represented by Bacteroidia and Clostridia. High similarity in bacterial diversity and composition was found for individuals from distinct groups, suggesting a negligible geographical effect at the fine spatial scale analyzed. No significant effect of host genotype heterozygosity levels on microbiota diversity was recovered, but a significant influence of genetic distance on microbiota community structure and composition was demonstrated. Our findings stress the importance of considering associations between host genetics and the microbiome and suggest that the analyzed populations host a similar microbiome composition. This detailed microbiome assessment can aid conservation actions, including future anthropogenic impact assessments and animal reintroductions.
... Social interactions, such as grooming, mating, and fecal consumption, can promote the horizontal transmission of gut microbiota among individuals within social groups. Social behavior can influence the composition and diversity of the gut microbiome, while the gut microbiome can also impact host behavior [96]. For example, dysbiosis induced by antibiotic treatment in mice was found to reduce the sexual attractiveness of females to males, highlighting the role of the MDEVs in shaping reproductive behavior [97]. ...
The animal gut microbiota, comprising a diverse array of microorganisms, plays a pivotal role in shaping host health and physiology. This review explores the intricate dynamics of the gut microbiome in animals, focusing on its composition, function, and impact on host–microbe interactions. The composition of the intestinal microbiota in animals is influenced by the host ecology, including factors such as temperature, pH, oxygen levels, and nutrient availability, as well as genetic makeup, diet, habitat, stressors, and husbandry practices. Dysbiosis can lead to various gastrointestinal and immune-related issues in animals, impacting overall health and productivity. Extracellular vesicles (EVs), particularly exosomes derived from gut microbiota, play a crucial role in intercellular communication, influencing host health by transporting bioactive molecules across barriers like the intestinal and brain barriers. Dysregulation of the gut–brain axis has implications for various disorders in animals, highlighting the potential role of microbiota-derived EVs in disease progression. Therapeutic approaches to modulate gut microbiota, such as probiotics, prebiotics, microbial transplants, and phage therapy, offer promising strategies for enhancing animal health and performance. Studies investigating the effects of phage therapy on gut microbiota composition have shown promising results, with potential implications for improving animal health and food safety in poultry production systems. Understanding the complex interactions between host ecology, gut microbiota, and EVs provides valuable insights into the mechanisms underlying host–microbe interactions and their impact on animal health and productivity. Further research in this field is essential for developing effective therapeutic interventions and management strategies to promote gut health and overall well-being in animals.
... In primates, individual variation in the intestinal microbiome is related to social structures and groups rather than habitat or diet, with adult microbiomes varying more with group www.nature.com/scientificreports/ affiliation than environment 49 . Furthermore, work on wild-caught vampire bats (Desmodus rotundus) that were merged into one colony upon capture suggests that social interactions influence the intestinal microbiome even when controlling for other factors 50 . ...
The intestinal microbiome plays an important role in mammalian health, disease, and immune function. In light of this function, recent studies have aimed to characterize the microbiomes of various bat species, which are noteworthy for their roles as reservoir hosts for several viruses known to be highly pathogenic in other mammals. Despite ongoing bat microbiome research, its role in immune function and disease, especially the effects of changes in the microbiome on host health, remains nebulous. Here, we describe a novel methodology to investigate the intestinal microbiome of captive Jamaican fruit bats (Artibeus jamaicensis). We observed a high degree of individual variation in addition to sex- and cohort-linked differences. The intestinal microbiome was correlated with intestinal metabolite composition, possibly contributing to differences in immune status. This work provides a basis for future infection and field studies to examine in detail the role of the intestinal microbiome in antiviral immunity.
... Although many primate studies found no strong evidence for kinship effects on gut microbiomes [38][39][40], a recent extensive study in baboons revealed that individuals inherit a significant portion of their gut communities from their ancestors [41]. Maternal relatives, whether residing in the same or different groups, exhibited more similar microbiota [42]. ...
Background
Captivity and artificial food provision are common conservation strategies for the endangered golden snub-nosed monkey (Rhinopithecus roxellana). Anthropogenic activities have been reported to impact the fitness of R. roxellana by altering their gut microbiota, a crucial indicator of animal health. Nevertheless, the degree of divergence in gut microbiota between different anthropogenically-disturbed (AD) R. roxellana and their counterparts in the wild has yet to be elucidated. Here, we conducted a comparative analysis of the gut microbiota across nine populations of R. roxellana spanning China, which included seven captive populations, one wild population, and another wild population subject to artificial food provision.
Results
Both captivity and food provision significantly altered the gut microbiota. AD populations exhibited common variations, such as increased Bacteroidetes and decreased Firmicutes (e.g., Ruminococcus), Actinobacteria (e.g., Parvibacter), Verrucomicrobia (e.g., Akkermansia), and Tenericutes. Additionally, a reduced Firmicutes/Bacteroidetes ratiosuggested diminished capacity for complex carbohydrate degradation in captive individuals. The results of microbial functional prediction suggested that AD populations displayed heightened microbial genes linked to vitamin and amino acid metabolism, alongside decreased genes associated antibiotics biosynthesis (e.g., penicillin, cephalosporin, macrolides, and clavulanic acid) and secondary metabolite degradation (e.g., naphthalene and atrazine). These microbial alterations implied potential disparities in the health status between AD and wild individuals. AD populations exhibited varying degrees of microbial changes compared to the wild group, implying that the extent of these variations might serve as a metric for assessing the health status of AD populations. Furthermore, utilizing the individual information of captive individuals, we identified associations between variations in the gut microbiota of R. roxellana and host age, as well as pedigree. Older individuals exhibited higher microbial diversity, while a closer genetic relatedness reflected a more similar gut microbiota.
Conclusions
Our aim was to assess how anthropogenic activities and host factors influence the gut microbiota of R. roxellana. Anthropogenic activities led to consistent changes in gut microbial diversity and function, while host age and genetic relatedness contributed to interindividual variations in the gut microbiota. These findings may contribute to the establishment of health assessment standards and the optimization of breeding conditions for captive R. roxellana populations.
