Effects of domestication on the gut microbiota parallel those of human industrialization

  1. Aspen T Reese  Is a corresponding author
  2. Katia S Chadaideh
  3. Caroline E Diggins
  4. Laura D Schell
  5. Mark Beckel
  6. Peggy Callahan
  7. Roberta Ryan
  8. Melissa Emery Thompson
  9. Rachel N Carmody  Is a corresponding author
  1. Department of Human Evolutionary Biology, Harvard University, United States
  2. Society of Fellows, Harvard University, United States
  3. Wildlife Science Center, United States
  4. Department of Anthropology, University of New Mexico, United States
7 figures, 1 table and 4 additional files

Figures

Figure 1 with 4 supplements
The mammalian gut microbiota carries a global signature of domestication.

(A) Sampling scheme for cross-species study. (B) Nonmetric multidimensional scaling (NMDS) ordination of Bray–Curtis dissimilarities illustrates a significant signal (p<0.001, R2 = 0.15, F = 6.081, …

Figure 1—figure supplement 1
Alternative factors associated with gut microbiota variation among wild and domesticated mammals.

Diet type (A), digestive physiology (B), and collection locale (C) are significantly associated (permutational MANOVAs) with variation in microbial community composition among wild and domesticated …

Figure 1—figure supplement 2
Microbial parameter comparisons between wild and domesticated mammals and between chimpanzees and humans.

Bray–Curtis nonmetric multidimensional scaling (NMDS) ordination shifts for domestication groups (A) and dyads (B), OTU richness (C), Shannon index (D), bacterial density (E), potential human …

Figure 1—figure supplement 3
Relatedness was correlated with ordination shifts but not dissimilarity within a dyad.

(A) The absolute value of shifts along nonmetric multidimensional scaling (NMDS) axis 1 for individuals relative to their dyad average was higher for dyads with a greater time since divergence …

Figure 1—figure supplement 4
Domestication explained few global gut microbial community characteristics in our cross-species dataset.

Potential pathogen richness (B) but not abundance (A) was significantly higher in wild animals. (C–E) Microbial density (quantified as copies of the 16S rRNA gene per gram feces [C]) and …

Figure 2 with 2 supplements
Gut microbial differences between wild and domesticated mice can be partially overcome by diet swap.

(A) Design scheme for fully factorial host taxon by diet mouse experiment (N = 10 laboratory mice or three wild mice per diet group). (B) Nonmetric multidimensional scaling (NMDS) ordination of …

Figure 2—figure supplement 1
Microbiota composition at all time points during the mouse diet swap experiment.

Nonmetric multidimensional scaling (NMDS) ordination of all time points illustrates significant effects (permutational MANOVA tests) of host taxon and diet on Bray–Curtis dissimilarity.

Figure 2—figure supplement 2
Select microbial and host metabolic parameters under mouse diet swap.

(A) Shannon index by experimental groups over time.(B) OTU richness by experimental groups over time. (C) Microbial load by experimental groups over time. (D) Total fecal production over 1 week …

Figure 3 with 1 supplement
Laboratory mice can be re-wilded through colonization with a wild gut microbial community.

(A) Design scheme for colonization/diet mouse experiment (N = 9–10 mice per treatment group). (B) Nonmetric multidimensional scaling (NMDS) ordination of Bray–Curtis dissimilarities showing changes …

Figure 3—figure supplement 1
Select microbial and host metabolic parameters under wild colonization treatment.

(A) Nonmetric multidimensional scaling (NMDS) ordination of all time points illustrates significant effects (permutational MANOVA tests) of colonization and diet treatment on Bray–Curtis …

Figure 4 with 2 supplements
Microbial differences between wild and domesticated canids can be partially overcome by diet shifts.

(A) Design scheme for fully factorial host taxon by diet canid experiment (N = 9 dogs or N = 10 wolves per diet group). (B) Nonmetric multidimensional scaling (NMDS) ordination of Bray–Curtis …

Figure 4—figure supplement 1
Microbiota composition at all time points during the canid diet swap experiment.

Nonmetric multidimensional scaling (NMDS) ordination of all time points illustrates significant effects (permutational MANOVA tests) of host taxon and diet on Bray–Curtis dissimilarity even after a …

Figure 4—figure supplement 2
Select microbial parameters under canid diet swap.

(A) Microbial loads of experimental groups over time.(B) Shannon index by experimental groups over time. (C) OTU richness differed between genotypes on day 0. * indicates p<0.05, Mann–Whitney U …

Figure 5 with 2 supplements
Differences in gut microbial communities between industrialized humans and wild chimpanzees parallel those observed between domesticated and wild mammals.

(A) Nonmetric multidimensional scaling (NMDS) ordination of Bray–Curtis dissimilarities in the gut microbiota illustrates that industrialized human populations (US and US Jha) exhibit similar trends …

Figure 5—figure supplement 1
Trends in gut microbial taxa previously linked to differing human lifestyles.

Abundance of gut microbial taxa previously identified as distinguishing among human lifestyles (Smits et al., 2017) trended in similar directions between domesticated and wild animals as between …

Figure 5—figure supplement 2
Dissimilarity in the gut microbiota among chimpanzees and humans.

Bray–Curtis dissimilarity among samples taken from captive zoo chimpanzees, wild chimpanzees, and human populations shows that the gut microbial communities of captive chimpanzees are more similar …

Author response image 1
Author response image 2

Tables

Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Biological sample (Bos taurus)FecesThis paperN = 9, sex unknown
Biological sample (Bison bison)FecesThis paperN = 20, sex unknown
Biological sample (Ovis aries)FecesThis paperN = 13, twelve females
Biological sample (Ovis canadensis)FecesThis paperN = 10, sex unknown
Biological sample (Sus scrofa domesticus)FecesThis paperN = 9, sex unknown
Biological sample (Sus scrofa)FecesThis paperN = 16, five females
Biological sample (Vicugna pacos)FecesThis paperN = 8, sex unknown
Biological sample (Vicugna vicugna)FecesThis paperN = 5, two females
Biological sample (Canis lupus familiaris)FecesThis paperComparative: N = 7, four females Experiment: N = 9, sex unknown
Biological sample (Canis lupus)FecesThis paperComparative: N = 9, sex unknown Experiment: N = 10, sex unknown
Biological sample (Oryctolagus cuniculus)FecesThis paperDomesticated: N = 11, four femalesWild: N = 12, sex unknown
Biological sample (Cavia porcellus)FecesThis paperN = 10, zero female
Biological sample (Cavia tschudii)FecesThis paperN = 11, sex unknown
Biological sample(Mus musculus)FecesThis paperComparative:
N = 9 (domesticated), zero female
N = 9 (wild), sex unknown
Experiments:
N = 49 (domesticated), zero female
N = 6 (wild), sex unknown
Biological sample (Rattus norvegicus)FecesThis paperDomesticated: N = 6, sex unknown
Biological sample (Rattus norvegicus)Intestinal sampleThis paperWild: N = 10, three females
Biological sample (Pan troglodytes)FecesThis paperWild: N = 7, seven females
Captive: N = 3, two females
Biological sample (Homo sapiens)FecesThis paperN = 7, five females
Sequence-based reagent515FCaporaso et al., 2011PCR primersGTGCCAGCMGCCGCGGTAA
Sequenced-based reagent806RCaporaso et al., 2012PCR primersGGACTACNVGGGTWTCTAAT
Software, algorithmRR Core TeamVersion 3.3
Software, algorithmQIIMECaporaso et al., 2010Version 1.8
Software, algorithmveganOksanen et al., 2017
Software, algorithmlme4Bates et al., 2015
Software, algorithmTimeTreeKumar et al., 2017http://timetree.org
Software, algorithmbootCanty and Ripley, 2020Version 1.3-25

Additional files

Supplementary file 1

Beta-diversity and nonmetric multidimensional scaling (NMDS) shift analyses were generally robust to the distance metric used and to subsetting the dataset.

https://cdn.elifesciences.org/articles/60197/elife-60197-supp1-v1.xlsx
Supplementary file 2

Expanded sampling metadata.

https://cdn.elifesciences.org/articles/60197/elife-60197-supp2-v1.xlsx
Supplementary file 3

Nutritional information for experimental diets.

https://cdn.elifesciences.org/articles/60197/elife-60197-supp3-v1.xlsx
Transparent reporting form
https://cdn.elifesciences.org/articles/60197/elife-60197-transrepform-v1.docx

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