Fecal Microbiomes: Baboons, bacteria, and biological clocks address an age-old question

Studying the fecal microbiota of wild baboons helps provide new insight into the factors that influence biological aging.
  1. Amanda D Melin  Is a corresponding author
  1. Department of Anthropology and Archaeology, University of Calgary, Canada

“Please be prepared to show your ID” is a sign you will often find in liquor stores, bars and other establishments selling age-restricted products. Indeed, it can be exceedingly hard to accurately estimate someone’s chronological age, which is based on their date of birth, just by looking at them. However, whether an individual appears younger or older than they are is more than just a skin-deep matter.

Recent advances in molecular biology have identified indicators of ‘biological age’, an estimate of how old your cells and systems really are (Jylhävä et al., 2017). Understanding the genetic, social, and environmental factors that influence the rate at which the body of an individual gets older is a longstanding research goal with important implications for improving healthy aging (Oblak et al., 2021). By comparing biological and chronological ages, for example, it becomes possible to identify individuals who age more slowly and uncover the external elements favoring the persistence of youthfulness.

Common methods for assessing the biological age of individuals often rely on examining telltale signs of aging in the genetic material extracted from blood or tissue samples (Duan et al., 2022). However, recent studies have highlighted age-associated changes in the composition of the gut microbiome, the complex community of bacteria and other microorganisms that inhabit the intestine and influence many biological systems in the body. This has led scientists to successfully generate human ‘microbiome clocks’ based on key bacterial taxa (Chen et al., 2022). A great benefit of gut microbiome research is that it relies on a substance – poop – that is readily available and non-invasive to collect. This has opened many research avenues impossible to explore with more traditional approaches, particularly in animal studies.

The immense complexity of human lives greatly complicates the study of how social and environmental factors influence aging, and researchers often turn to animal models such as primates to overcome these limitations (Chiou et al., 2020). Baboons, for instance, share many similarities with humans when it comes to their genomes, physiologies, ecologies, behaviors, and social lives. By providing uninterrupted and detailed biological and behavioral insights into a wild population of yellow baboons (Papio cynocephalus) over several decades, the Amboseli Baboon Research Project has provided impactful contributions to the field (Alberts and Altmann, 2012). This includes helping to establish how social and physical attributes of an environment shape the composition and biological functions of the gut microbiome (Tung et al., 2015; Grieneisen et al., 2021). Now, in eLife, Mauna Dasari (University of Notre Dame and University of Pittsburgh), Elizabeth Archie (Notre Dame) and colleagues at various institutes in the United States, Germany and Canada report how baboon microbiome clocks can be established from fecal samples, and how these are influenced by various biological, social and ecological factors (Dasari et al., 2024; Figure 1).

Baboon microbiome clocks can be established from fecal samples.

Dasari et al. took advantage of data collected over several decades on a wild population of yellow baboons living in the Amboseli region to examine variation in biological age among individuals. They demonstrated that it was possible to use fecal samples to infer microbiome clocks based on age-related changes in the composition of various bacterial taxa (red, green, blue and purple icons within the clocks). In turn, these clocks made it possible to investigate the biological, social and environmental pressures that shape the pace at which an individual ages.

Image credit: Alyssa Bohart (CC BY 4.0).

The team used a supervised machine learning technique to predict the age of a baboon at the time of sampling based on the bacterial taxa present in its feces. The dataset included 13,563samples repeatedly collected from 479 baboons over 14years. While biological clocks established using information from the DNA of an individual remained the most precise, on average the fecal microbiome approach correctly estimated the chronological age of a baboon within about a two-year range, with the predictions for males being slightly better than for females. These results were more accurate than those obtained in the same population using some other aging biomarkers, such as body mass index or blood cell counts.

Clear sex differences in biological aging also emerged (a result consistent with previous studies on non-microbiome clocks), with sexually mature males being microbially older for their chronological age than females were. High-ranking males also had older microbiome clocks than their low-ranking counterparts, potentially due to the age-accelerating effects of the high energy requirements associated with having to physically fight to obtain and preserve their status. These results add to previous findings suggesting that dominant males are biologically old for their chronological age (Anderson et al., 2021). More unexpectedly, a similar pattern was also discovered in females, which tend to inherit their social rank rather than fight for it. The team predicted that low-ranking females, who experience more stressful conditions due to reduced access to food and other resources, would age more rapidly at a biological level – yet it was the higher-ranking females that had ‘older’ microbial features.

The gap between microbial and chronological ages varied greatly across baboons who, like humans, encounter differing experiences throughout their lives. For example, adverse events that take place early in life – such as losing a mother or living through extreme droughts as an infant – can have long-lasting consequences for development, aging and lifespan (Anderson et al., 2024). Counterintuitively, Dasari et al. found that early experiences of droughts or maternal isolation had no clear impact on females and were in fact linked to ‘younger’ microbiomes in males. This is especially surprising given that female samples collected during dry periods showed ‘older’ microbial signals than those obtained during the wet season, which presents fewer challenges for survival. Finally, none of the microbiome variables examined had predictive potential regarding mortality or an individual’s ability to attain major developmental milestones. Taken together, these findings indicate that periods of ecological stress can accelerate biological aging, but that current or recent conditions have a greater impact on biological age than those encountered early in life.

The work by Dasari et al. generates important insights into the processes influencing biological aging, and it is sure to inspire many future investigations, in particular into the potential impact of social networks. By showing that reliable biological clocks can be established using fecal microbiome analyses (and therefore easily accessible samples), this study may make it easier for researchers to investigate facets of aging within and across a variety of species.

References

  1. Book
    1. Alberts SC
    2. Altmann J
    (2012) The Amboseli Baboon Research Project: 40 years of continuity and change
    In: Alberts SC, editors. Long-Term Field Studies of Primates. Berlin, Heidelberg: Springer. pp. 261–287.
    https://doi.org/10.1007/978-3-642-22514-7

Article and author information

Author details

  1. Amanda D Melin

    Amanda D Melin is in the Department of Anthropology and Archaeology, University of Calgary, Calgary, Canada

    For correspondence
    amanda.melin@ucalgary.ca
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0612-2514

Publication history

  1. Version of Record published:

Copyright

© 2024, Melin

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 364
    views
  • 35
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Amanda D Melin
(2024)
Fecal Microbiomes: Baboons, bacteria, and biological clocks address an age-old question
eLife 13:e104715.
https://doi.org/10.7554/eLife.104715
  1. Further reading

Further reading

    1. Ecology
    2. Evolutionary Biology
    Justine Boutry, Océane Rieu ... Fréderic Thomas
    Research Article

    While host phenotypic manipulation by parasites is a widespread phenomenon, whether tumors, which can be likened to parasite entities, can also manipulate their hosts is not known. Theory predicts that this should nevertheless be the case, especially when tumors (neoplasms) are transmissible. We explored this hypothesis in a cnidarian Hydra model system, in which spontaneous tumors can occur in the lab, and lineages in which such neoplastic cells are vertically transmitted (through host budding) have been maintained for over 15 years. Remarkably, the hydras with long-term transmissible tumors show an unexpected increase in the number of their tentacles, allowing for the possibility that these neoplastic cells can manipulate the host. By experimentally transplanting healthy as well as neoplastic tissues derived from both recent and long-term transmissible tumors, we found that only the long-term transmissible tumors were able to trigger the growth of additional tentacles. Also, supernumerary tentacles, by permitting higher foraging efficiency for the host, were associated with an increased budding rate, thereby favoring the vertical transmission of tumors. To our knowledge, this is the first evidence that, like true parasites, transmissible tumors can evolve strategies to manipulate the phenotype of their host.

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease
    Zach Hensel
    Short Report

    Accurate estimation of the effects of mutations on SARS-CoV-2 viral fitness can inform public-health responses such as vaccine development and predicting the impact of a new variant; it can also illuminate biological mechanisms including those underlying the emergence of variants of concern. Recently, Lan et al. reported a model of SARS-CoV-2 secondary structure and its underlying dimethyl sulfate reactivity data (Lan et al., 2022). I investigated whether base reactivities and secondary structure models derived from them can explain some variability in the frequency of observing different nucleotide substitutions across millions of patient sequences in the SARS-CoV-2 phylogenetic tree. Nucleotide basepairing was compared to the estimated ‘mutational fitness’ of substitutions, a measurement of the difference between a substitution’s observed and expected frequency that is correlated with other estimates of viral fitness (Bloom and Neher, 2023). This comparison revealed that secondary structure is often predictive of substitution frequency, with significant decreases in substitution frequencies at basepaired positions. Focusing on the mutational fitness of C→U, the most common type of substitution, I describe C→U substitutions at basepaired positions that characterize major SARS-CoV-2 variants; such mutations may have a greater impact on fitness than appreciated when considering substitution frequency alone.