Age Patterning in Wild Chimpanzee Gut Microbiota Diversity Reveals Differences from Humans in Early Life

Reese, Aspen T.; Phillips-Garcia, Sarah; Owens, L.; Venable, Emily M.; Langergraber, Kevin E.; Machanda, Zarin; Mitani, John C.; Muller, Martin N.; Watts, David P.; Wrangham, Richard W.; Goldberg, Tony L.; Thompson, Melissa Emery; Carmody, Rachel N.

doi:10.1016/j.cub.2020.10.075

Cited by 40 publications

(49 citation statements)

References 71 publications

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“…Consistent with previous studies in humans and rhesus macaques but opposite a recent study in chimpanzees [51,52], alpha diversity of the vervet monkey infant gut microbiome was lowest during early life, converging rapidly toward maternal gut microbiome levels by 4 months old. Although a less diverse microbiome during adulthood can indicate microbiome dysbiosis [53,54], reduced diversity during development may instead reflect specialization of the gut microbiome for specific functions.…”

Section: Discussionsupporting

confidence: 90%

Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

Petrullo

Baniel

et al. 2021

Preprint

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Background: Maternal parity is associated with variation in infant growth across mammals, but the mechanisms underlying this relationship are unclear. Given emerging links between growth and the microbiome, and the importance of maternal microbiota in establishing this community, the assembly of the infant gut microbiome may be a mediator of parity effects on infant growth. Results: Here, we analyzed 118 fecal and milk samples from mother-infant vervet monkey dyads across the first 6 months postpartum in a population with high growth-associated infant mortality. Despite poorer milk production, infants born to low parity females were larger at 6 months of age than their counterparts and exhibited divergent patterns in gut microbiome assembly. Gut microbiome alpha diversity increased rapidly from the first days of life to 4 months old in all infants, but infants born to low parity females exhibited reduced gut microbiome alpha diversity during early life. At the taxonomic level, infants broadly exhibited a shift from Bacteroides fragilis to Prevotella dominance. Infants of low parity females housed more B. fragilis in their guts, and B. fragilis dominance drove reduced alpha diversity. Maternal vertical transmission to the infant gut was greater from milk than from the maternal gut, and was greatest among infants born to low parity females. B. fragilis was 15-fold more abundant in milk than in the maternal gut and was greater in the milk of low parity females, suggesting that milk may be the primary maternal reservoir of B. fragilis. Path analyses demonstrated that both infant gut alpha diversity and B. fragilis mediated parity effects on postnatal growth: infants were larger at 6 months old if they exhibited reduced alpha diversity and a greater relative abundance of B. fragilis during early life. Conclusion: The first days of life are a critical period of infant gut microbiome organization during which the establishment of a less diverse, milk-oriented microbial community abundant in B. fragilis promotes growth among infants born to reproductively inexperienced females.

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Section: Discussionsupporting

confidence: 90%

Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

Petrullo

Baniel

et al. 2021

Preprint

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“…The broad dynamic of microbial colonization in geladas presents many similarities with previous reports on humans [2,5,8] and other mammals ( [10,37,73], but see [74]). We observed a low initial number of microbes and a rapid increase in microbial diversity in the first seven months of life, followed by more gradual changes in microbial composition until weaning (~17 months).…”

Section: Discussionsupporting

confidence: 81%

“…Although studies on host-associated microbial communities in wild primates are emerging, many remain limited in scope, hampered by cross-sectional samples and small sample sizes of unweaned infants (particularly in the first few weeks of life), which together prevent longitudinal characterization of gut microbial colonization processes [72][73][74][75]. Here, we used dense crosssectional and longitudinal monitoring to characterize gut microbial colonization during the first three years of life and assess the role of maternal effects in shaping offspring maturation trajectories in wild gelada monkeys (Theropithecus gelada).…”

Section: Introductionmentioning

confidence: 99%

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Baniel

Petrullo

Mercer

et al. 2021

Preprint

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Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

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“…Fledglings had a significantly different GM composition compared to other age classes, despite the fact that they are still reliant on food from their parents and remain in their natal territory. Development has been shown to strongly influence GM composition in humans and other primates [28,109] and, although few studies have investigated changes in the GM across the life course of birds, several studies have identified differences between the GM of nestlings versus adult individuals [77,110]. Sub-adult Seychelles warblers also had a more variable GM community compared to other age classes.…”

Section: Host and Environmental Factors Influencing Gm Beta Diversitymentioning

confidence: 99%

“…Several studies have demonstrated interspecific differences in GM characteristics [17][18][19], and also variation between groups [20][21][22] or individuals [23][24][25] within the same natural population. Most of these studies have focussed on investigating the drivers of intraspecific variation in the bacterial component of the GM, identifying a suite of environmental factors that can influence this, including habitat quality and dietary differences [24][25][26], as well as host-related traits, such as age, sex, and host genotype [23,27,28]. However, very few studies have investigated the consequences of individual GM variation for host health and fitness (survival and/or reproductive success) in natural populations.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population

Worsley

Davies

Mannarelli

et al. 2021

Preprint

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Background: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition and survival using data from the long-term study of a discrete natural population of the Seychelles warbler ( Acrocephalus sechellensis ) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons. Results: We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (7% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between individuals that survived, versus those that had died by the following breeding season. Individuals that died carried reduced abundances of beneficial taxa in the bacterial order Clostridiales , but increased abundances of taxa that are known to be opportunistic pathogens (e.g. members of the Chloroflexi and Propionibacteriales ). However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition. Conclusions: These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild, although whether changes in bacterial abundance contribute to, or are only correlated with, the differential survival observed remains unclear. Importantly, it suggests that components of the GM may be under selection, and, thus, could have the potential to influence the evolution of host species living in natural populations.

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Age Patterning in Wild Chimpanzee Gut Microbiota Diversity Reveals Differences from Humans in Early Life

Cited by 40 publications

References 71 publications

Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population

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