Title: Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors
AbstractObjectives
Environmental and ecological factors, such as geographic range, anthropogenic pressure, group identity, and feeding behavior are known to influence the gastrointestinal microbiomes of great apes. However, the influence of individual host traits such as age and sex, given specific dietary and social constraints, has been less studied. The objective of this investigation was to determine the associations between an individual's age and sex on the diversity and composition of the gut microbiome in wild western lowland gorillas.
Materials and Methods
Publicly available 16S rRNA data generated from fecal samples of different groups ofGorilla gorillagorillain the Central African Republic were downloaded and bioinformatically processed. The groups analyzed included habituated, partially habituated and unhabituated gorillas, sampled during low fruit (dry,n = 28) and high fruit (wet,n = 82) seasons. Microbial community analyses (alpha and beta diversity and analyses of discriminant taxa), in tandem with network‐wide approaches, were used to (a) mine for specific age and sex based differences in gut bacterial community composition and to (b) asses for gut community modularity and bacterial taxa with potential functional roles, in the context of seasonal food variation, and social group affiliation.
Results
Both age and sex significantly influenced gut microbiome diversity and composition in wild western lowland gorillas. However, the largest differences were observed between infants and adults in habituated groups and between adults and immature gorillas within all groups, and across dry and wet seasons. Specifically, although adults always showed greater bacterial richness than infants and immature gorillas, network‐wide analyses showed higher microbial community complexity and modularity in the infant gorilla gut. Sex‐based microbiome differences were not evident among adults, being only detected among immature gorillas.
Conclusions
The results presented point to a dynamic gut microbiome inGorillaspp., associated with ontogeny and individual development. Of note, the gut microbiomes of breastfeeding infants seemed to reflect early exposure to complex, herbaceous vegetation. Whether increased compositional complexity of the infant gorilla gut microbiome is an adaptive response to an energy‐limited diet and an underdeveloped gut needs to be further tested. Overall, age and sex based gut microbiome differences, as shown here, maybe mainly attributed to access to specific feeding sources, and social interactions between individuals within groups.
Ruff, Christopher B.; Burgess, M. Loring; Junno, Juho‐Antti; Mudakikwa, Antoine; Zollikofer, Christophe P. E.; Ponce de León, Marcia S.; McFarlin, Shannon C.(
, American Journal of Physical Anthropology)
AbstractObjectives
The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas.
Materials and Methods
A total of 281 wild‐collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas(G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross‐sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development.
Results
Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals.
Conclusion
Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.
Muletz‐Wolz, Carly R.; Kurata, Naoko P.; Himschoot, Elizabeth A.; Wenker, Elizabeth S.; Quinn, Elizabeth A.; Hinde, Katie; Power, Michael L.; Fleischer, Robert C.(
, American Journal of Primatology)
Abstract
Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut‐brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high‐throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.
Robbins, Martha M.; Akantorana, Moses; Arinaitwe, Joseph; Breuer, Thomas; Manguette, Marie; McFarlin, Shannon; Meder, Angela; Parnell, Richard; Richardson, Jack L.; Stephan, Claudia; et al(
, American Journal of Biological Anthropology)
AbstractObjectives
Several theories have been proposed to explain the impact of ecological conditions on differences in life history variables within and between species. Here we compare female life history parameters of one western lowland gorilla population(Gorilla gorilla gorilla) and two mountain gorilla populations(Gorilla beringei beringei).
Materials and Methods
We compared the age of natal dispersal, age of first birth, interbirth interval, and birth rates using long‐term demographic datasets from Mbeli Bai (western gorillas), Bwindi Impenetrable National Park and the Virunga Massif (mountain gorillas).
Results
The Mbeli western gorillas had the latest age at first birth, longest interbirth interval, and slowest surviving birth rate compared to the Virunga mountain gorillas. Bwindi mountain gorillas were intermediate in their life history patterns.
Discussion
These patterns are consistent with differences in feeding ecology across sites. However, it is not possible to determine the evolutionary mechanisms responsible for these differences, whether a consequence of genetic adaptation to fluctuating food supplies (“ecological risk aversion hypothesis”) or phenotypic plasticity in response to the abundance of food (“energy balance hypothesis”). Our results do not seem consistent with the extrinsic mortality risks at each site, but current conditions for mountain gorillas are unlikely to match their evolutionary history. Not all traits fell along the expected fast‐slow continuum, which illustrates that they can vary independently from each other (“modularity model”). Thus, the life history traits of each gorilla population may reflect a complex interplay of multiple ecological influences that are operating through both genetic adaptations and phenotypic plasticity.
Ostrofsky, Kelly_R; Robbins, Martha_M(
, American Journal of Physical Anthropology)
AbstractObjectives
Availability of fruit is an important factor influencing variation in great ape foraging strategies and activity patterns. This study aims to quantify how frugivory influences activity budgets across age‐sex classes of mountain gorillas in Bwindi Impenetrable National Park, Uganda.
Materials and methods
Daily proportions of fruit‐feeding and activity budgets were calculated using 6 years of observational data on four habituated groups. We fitted generalized linear mixed models to test for age‐sex differences in the amount of fruit‐feeding, and to test whether these factors influence the proportion of time spent feeding, resting, and traveling.
Results
Bwindi mountain gorillas spent on average 15% of feeding time consuming fruit, with monthly variation ranging from 0 to 70%. Greater amounts of fruit‐feeding were associated with more time feeding and traveling, and less time resting. Immatures tended to spend more feeding time on fruit than adults, but less overall time feeding and more time traveling. There were no significant differences in the amount of fruit‐feeding and overall feeding time between adult females and silverback males, despite differences in body size.
Discussion
This study confirms that gorillas are frugivorous, and only the Virunga mountain gorilla population can be characterized as highly folivorous. Along with other frugivorous great apes, Bwindi mountain gorillas alter their activity patterns in response to varying amounts of fruit in their diet. A better understanding of how variable ecological conditions can drive diversity even within a subspecies has important implications for understanding relationships between ecology, body size, and foraging strategies in great apes.
Lane, Avery A.; McGuire, Michelle K.; McGuire, Mark A.; Williams, Janet E.; Lackey, Kimberly A.; Hagen, Edward H.; Kaul, Abhishek; Gindola, Debela; Gebeyehu, Dubale; Flores, Katherine E.; et al(
, American Journal of Physical Anthropology)
AbstractObjectives
Establishment and development of the infant gastrointestinal microbiome (GIM) varies cross‐culturally and is thought to be influenced by factors such as gestational age, birth mode, diet, and antibiotic exposure. However, there is little data as to how the composition of infants' households may play a role, particularly from a cross‐cultural perspective. Here, we examined relationships between infant fecal microbiome (IFM) diversity/composition and infants' household size, number of siblings, and number of other household members.
Materials and methods
We analyzed 377 fecal samples from healthy, breastfeeding infants across 11 sites in eight different countries (Ethiopia, The Gambia, Ghana, Kenya, Peru, Spain, Sweden, and the United States). Fecal microbial community structure was determined by amplifying, sequencing, and classifying (to the genus level) the V1–V3 region of the bacterial 16S rRNA gene. Surveys administered to infants' mothers identified household members and composition.
Results
Our results indicated that household composition (represented by the number of cohabitating siblings and other household members) did not have a measurable impact on the bacterial diversity, evenness, or richness of the IFM. However, we observed that variation in household composition categories did correspond to differential relative abundances of specific taxa, namely:Lactobacillus,Clostridium,Enterobacter, andKlebsiella.
Discussion
This study, to our knowledge, is the largest cross‐cultural study to date examining the association between household composition and the IFM. Our results indicate that the social environment of infants (represented here by the proxy of household composition) may influence the bacterial composition of the infant GIM, although the mechanism is unknown. A higher number and diversity of cohabitants and potential caregivers may facilitate social transmission of beneficial bacteria to the infant gastrointestinal tract, by way of shared environment or through direct physical and social contact between the maternal–infant dyad and other household members. These findings contribute to the discussion concerning ways by which infants are influenced by their social environments and add further dimensionality to the ongoing exploration of social transmission of gut microbiota and the “old friends” hypothesis.
Pafčo, Barbora, Sharma, Ashok_K, Petrželková, Klára_J, Vlčková, Klára, Todd, Angelique, Yeoman, Carl_J, Wilson, Brenda_A, Stumpf, Rebecca, White, Bryan_A, Nelson, Karen_E, Leigh, Steven, and Gomez, Andres. Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors. American Journal of Physical Anthropology 169.3 Web. doi:10.1002/ajpa.23842.
Pafčo, Barbora, Sharma, Ashok_K, Petrželková, Klára_J, Vlčková, Klára, Todd, Angelique, Yeoman, Carl_J, Wilson, Brenda_A, Stumpf, Rebecca, White, Bryan_A, Nelson, Karen_E, Leigh, Steven, & Gomez, Andres. Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors. American Journal of Physical Anthropology, 169 (3). https://doi.org/10.1002/ajpa.23842
Pafčo, Barbora, Sharma, Ashok_K, Petrželková, Klára_J, Vlčková, Klára, Todd, Angelique, Yeoman, Carl_J, Wilson, Brenda_A, Stumpf, Rebecca, White, Bryan_A, Nelson, Karen_E, Leigh, Steven, and Gomez, Andres.
"Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors". American Journal of Physical Anthropology 169 (3). Country unknown/Code not available: Wiley Blackwell (John Wiley & Sons). https://doi.org/10.1002/ajpa.23842.https://par.nsf.gov/biblio/10461569.
@article{osti_10461569,
place = {Country unknown/Code not available},
title = {Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors},
url = {https://par.nsf.gov/biblio/10461569},
DOI = {10.1002/ajpa.23842},
abstractNote = {Abstract ObjectivesEnvironmental and ecological factors, such as geographic range, anthropogenic pressure, group identity, and feeding behavior are known to influence the gastrointestinal microbiomes of great apes. However, the influence of individual host traits such as age and sex, given specific dietary and social constraints, has been less studied. The objective of this investigation was to determine the associations between an individual's age and sex on the diversity and composition of the gut microbiome in wild western lowland gorillas. Materials and MethodsPublicly available 16S rRNA data generated from fecal samples of different groups ofGorilla gorillagorillain the Central African Republic were downloaded and bioinformatically processed. The groups analyzed included habituated, partially habituated and unhabituated gorillas, sampled during low fruit (dry,n = 28) and high fruit (wet,n = 82) seasons. Microbial community analyses (alpha and beta diversity and analyses of discriminant taxa), in tandem with network‐wide approaches, were used to (a) mine for specific age and sex based differences in gut bacterial community composition and to (b) asses for gut community modularity and bacterial taxa with potential functional roles, in the context of seasonal food variation, and social group affiliation. ResultsBoth age and sex significantly influenced gut microbiome diversity and composition in wild western lowland gorillas. However, the largest differences were observed between infants and adults in habituated groups and between adults and immature gorillas within all groups, and across dry and wet seasons. Specifically, although adults always showed greater bacterial richness than infants and immature gorillas, network‐wide analyses showed higher microbial community complexity and modularity in the infant gorilla gut. Sex‐based microbiome differences were not evident among adults, being only detected among immature gorillas. ConclusionsThe results presented point to a dynamic gut microbiome inGorillaspp., associated with ontogeny and individual development. Of note, the gut microbiomes of breastfeeding infants seemed to reflect early exposure to complex, herbaceous vegetation. Whether increased compositional complexity of the infant gorilla gut microbiome is an adaptive response to an energy‐limited diet and an underdeveloped gut needs to be further tested. Overall, age and sex based gut microbiome differences, as shown here, maybe mainly attributed to access to specific feeding sources, and social interactions between individuals within groups.},
journal = {American Journal of Physical Anthropology},
volume = {169},
number = {3},
publisher = {Wiley Blackwell (John Wiley & Sons)},
author = {Pafčo, Barbora and Sharma, Ashok_K and Petrželková, Klára_J and Vlčková, Klára and Todd, Angelique and Yeoman, Carl_J and Wilson, Brenda_A and Stumpf, Rebecca and White, Bryan_A and Nelson, Karen_E and Leigh, Steven and Gomez, Andres},
}
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