Living inside our gastrointestinal tracts is a large and diverse community of bacteria called the gut microbiota that plays an active role in basic body processes like metabolism and immunity. Much of our current understanding of the gut microbiota has come from laboratory animals like mice, which have very different gut bacteria to mice living in the wild. However, it was unclear whether this difference in microbes was due to domestication, and if it could also be seen in other domesticated-wild pairs, like pigs and wild boars or dogs and wolves.

A few existing studies have compared the gut bacteria of two species in a domesticated-wild pair. But, studies of isolated pairs cannot distinguish which factors are responsible for altering the microbiota of domesticated animals. To overcome this barrier, Reese et al. sequenced microbial DNA taken from fecal samples of 18 species of wild and related domesticated mammals.

The results showed that while domesticated animals have different sets of bacteria in their guts, leaving the wild has changed the gut microbiota of these diverse animals in similar ways. To explore what causes these shared patterns, Reese et al. swapped the diets of two domesticated-wild pairs: laboratory and wild mice, and dogs and wolves. They found this change in diet shifted the gut bacteria of the domesticated species to be more similar to that of their wild counterparts, and vice versa. This suggests that altered eating habits helped drive the changes domestication has had on the gut microbiota.

To find out whether these differences also occur in humans, Reese et al. compared the gut microbes of chimpanzees with the microbiota of people living in different environments. The gut microbial communities of individuals from industrialized populations had more in common with those of domesticated animals than did the microbes found in chimpanzees or humans from non-industrialized populations. This suggests that industrialization and domestication have had similar effects on the gut microbiota, likely due to similar kinds of environmental change.

Domesticated animals are critical for the economy and health, and understanding the central role gut microbes play in their biology could help improve their well-being. Given the parallels between domestication and industrialization, knowledge gained from animal pairs could also shed light on the human gut microbiota. In the future, these insights could help identify new ways to alter the gut microbiota to improve animal or human health.

Industrialized, agrarian, and foraging human populations differ along numerous ecological dimensions, including diet, physical activity, the size and nature of social networks, pathogen exposure, types and intensities of medical intervention, and reproductive patterns. Such changes have resulted in large shifts in the gut microbiota in industrialized populations relative to non-industrialized populations or closely related primates (De Filippo et al., 2010; Moeller et al., 2014; Moeller, 2017; Smits et al., 2017), including reductions in alpha-diversity and changes in composition that have been implicated in the rise of various metabolic and immunological diseases (Ley et al., 2006; Cox et al., 2014; Kamada et al., 2013). Many aspects of ecology that now differ between industrialized and non-industrialized human populations were similarly altered during the process of animal domestication (Zeder, 2012). For example, domestic animals often consume less diverse, more easily digestible diets than their wild relatives, expend less energy to achieve adequate (or excess) caloric intake, live in comparatively static and high-density groups, and can be subject to modern medical interventions including antibiotic treatment (McClure, 2013). Although industrialization and domestication are fundamentally different processes, the ecological parallels between human industrialization and animal domestication suggest that the gut microbiota of diverse domesticated animals may differ in consistent ways from those of their wild progenitors, and further, that their differences may resemble those observed between industrialized and non-industrialized human populations.

Many of the altered ecological features experienced by industrialized humans and domesticated animals have been independently observed to impact the gut microbiota, including diet (David et al., 2014; Carmody et al., 2015), physical activity (Allen et al., 2018; Lamoureux et al., 2017), the size and nature of social networks (Dill-McFarland et al., 2019; Antwis et al., 2018), antibiotic use (Bokulich et al., 2016; Cho et al., 2012), and changes in birthing and lactation practices (Bokulich et al., 2016; Li et al., 2018). The effects of these features on gut microbiota composition are often found to match or exceed the effects of genetic variation (Carmody et al., 2015; Rothschild et al., 2018), which is also routinely modified by domestication. As such, ecological shifts under domestication might be expected to lead to gut microbial differentiation between domesticated animals and their wild counterparts. To this end, wild mice have been shown to differ from laboratory mice in gut microbial composition (Kreisinger et al., 2014; Rosshart et al., 2017). Similarly, a comparison of domesticated horses and wild Przewalski’s horses in adjacent Mongolian grasslands found that the wild animals harbored compositionally distinct, and overall more diverse, gut microbial communities (Metcalf et al., 2017). However, to date, no general survey has been conducted to characterize the global effects of domestication on the gut microbiota.

Apart from the pressures of ecological change that domestic animals experience in human environments, animal domestication has also entailed strong artificial selection for phenotypes desirable to humans, such as rapid growth and docility in agricultural animals, reliable reproduction and stress resistance in laboratory animals, and unique physical and/or behavioral attributes in companion animals. Although targeted phenotypes differ based on the species under domestication, all domesticated mammals share the legacy of having been intentionally or indirectly selected for tameness (Wilkins et al., 2014). This selection has been argued to have resulted in convergent morphological and physiological features across domesticated mammals that are collectively referred to as ‘domestication syndrome’ – including, for instance, reductions in brain size and tooth size, depigmentation, altered production of hormones and neurotransmitters, and retention of juvenile behaviors into adulthood – with the pleiotropic nature of these effects thought to be mediated by changes in neural crest cells (Wilkins et al., 2014). Therefore, to the extent that gut microbiota is dependent on host biology, we might additionally expect domestication to have shaped the gut microbiome in similar, potentially convergent, ways across diverse mammalian lineages. Such microbiota-structuring contributions ascribable to evolutionary rather than ecological forces have the potential to be much greater in and/or unique to domesticated animals relative to industrialized human populations since the process of domestication has been advancing for much longer than industrialization.

Here, we assess the effects of domestication on the mammalian gut microbiota, perform controlled dietary experiments that attempt to distinguish between the relative roles of ecology and genetics in driving these patterns, and compare the effects of domestication to those of human industrialization. While we focus primarily on the impacts of domestication on the mammalian gut microbiota, we include analyses of industrialized and non-industrialized human populations because much is known about the effects of industrialization on the gut microbiota and as such it can serve as a benchmark ecological process for domestication. In addition, to explore the extent to which deeper evolutionary history affects these patterns, we also compare humans to chimpanzees (Pan troglodytes), one of our two closest living relatives and arguably the better referential model for the last common ancestor between Pan and Homo (Muller et al., 2017). Early Homo sapiens is thought to have undergone a form of self-domestication as a result of selection against aggression (Wrangham, 2018; Theofanopoulou et al., 2017), suggesting that there could likewise be parallels between the gut microbial signatures of animal domestication and Pan–Homo speciation.

We predict that (i) gut microbial communities will differ between domesticated animals and their wild counterparts, (ii) gut microbial communities of diverse domesticated animals may exhibit convergent characteristics in a microbial counterpart to the physiological domestication syndrome (Wilkins et al., 2014), and (iii) gut microbial changes observed with domestication may parallel contrasts observed between chimpanzees and humans. In addition, to the extent that domestication effects are driven by ecology rather than host phylogenetic distance, we should expect (iv) experimental manipulation of ecology to overcome differences in the gut microbiota between closely related hosts, and (v) the gut microbiota of domesticated animals will share more features with industrialized human populations than with non-industrialized human populations.

Identifying the factors shaping the gut microbiota of domesticated animals will provide insights into the ecology of host-associated microbial communities and their impact on health. Domesticated animals serve as reservoirs for zoonotic diseases (Morand et al., 2014; Wolfe et al., 2007; Cleaveland et al., 2001; Han et al., 2016) and carriers of antibiotic-resistant bacteria (Sayah et al., 2005; EFFORT Group et al., 2018). Furthermore, the ecological impacts of domestication on the gut microbiota could conceivably contribute to the unique health problems experienced by captive (Hosey et al., 2009) and domesticated animals (Timoney et al., 1988). Differences between domesticated and wild animal microbiota may also manifest in poor translatability between laboratory studies and the real world (Leung et al., 2018; Beura et al., 2016). Finally, the convergent nature of many ecological shifts experienced by domesticated animals and industrialized human populations suggests that domesticated animals may provide a uniquely useful model for studying the microbially mediated health impacts of rapid environmental change that results in mismatch between host, microbiota, and/or environment, a situation thought to apply to humans in industrialized settings (Sonnenburg and Sonnenburg, 2019). Understanding what shapes the domesticated microbiota may therefore identify routes to improve experimental models, animal condition, and human health.

Our data demonstrate that while domestication has not led to a convergent ‘domesticated microbiota,’ there is nevertheless a significant signal of domestication on gut community composition across diverse mammalian hosts. Furthermore, our experimental and cross-sectional analyses suggest that the domestication effect can, in large part, be ascribed to environmental rather than genetic changes. As in many comparative microbiota studies, host taxonomy was responsible for the largest component of variation in our cross-species analyses, but the contribution of domestication status was comparable to those of diet type and host physiology, factors previously identified as key drivers of the mammalian gut microbiota (Ley et al., 2008; McKenzie et al., 2017). Experimental diet intervention in wild/domesticated pairs reduced gut microbial dissimilarity and alpha-diversity differences between members of the dyad over short time scales. However, differences due to loss or gain of taxa during domestication could not be overcome by diet shifts alone, necessitating experimental recolonization. Together, these results indicate that domestication has played a large role in shaping the microbiota and, through husbandry practices, likely continues to do so today, suggesting that studying variations in animal husbandry practices may illuminate new levers for manipulating the mammalian gut microbiota (Velazquez et al., 2019; Villarino et al., 2016; Schmidt et al., 2019).

Although there are many shared features of contemporary ecology and historic artificial selection on domestic animals, it is perhaps unsurprising that domestication has not produced a single, convergent domesticated gut microbiota. The animals we characterized represent a diverse set of lineages in the mammalian clade, and thus their microbiota also differ due to variation in factors such as gut structure and size, passage rate, diet, and biogeography (Ley et al., 2008; Youngblut et al., 2019). While the domestication signal was comparable in magnitude to those of gut physiology and diet type, it does not mask those fundamental structuring forces. Furthermore, the particulars of a domesticated lineage can help clarify what aspects of ecology are most salient to the domestication effect. Cases where domestication effects are weaker in our comparative study generally consist of animals where the ecological change associated with domestication has been small – for example, sheep and pigs, whose diets may be quite similar to their wild progenitors, at least when kept in the non-industrialized agricultural settings that were sampled (McClure, 2013) – or where ecological changes are in the opposite direction from the domesticated norm – for example, canids, where the domesticate diet typically involves lower protein and higher carbohydrate levels than wild diets, instead of the higher protein levels seen in most laboratory or farm animals (Axelsson et al., 2013).

Our reciprocal diet experiments in mice and canids substantiate our claim that ecology plays a predominant role in shaping the domesticated gut microbiota. However, they do not pinpoint the mechanism(s) for these effects. Variability in diet or other aspects of ecology and their concomitant effects on host physiology (e.g., passage rate) can alter microbial composition or abundance through changes in the selective landscape that microbes experience and changes in environmental exposure (David et al., 2014; Carmody et al., 2019). Animals may experience altered bacterial colonization, leading directly to changes in composition, and/or viral colonization, which could then alter the bacterial community if new bacteriophages target gut bacteria or if eukaryotic viruses activate the host immune system, leading to transformations in the gut environment. That the gut microbial impacts of change in a single ecological variable like diet were sufficiently profound to balance those of host taxon identity suggests that suites of ecological variables changing together, such as during domestication or industrialization, may have collectively exerted an even larger influence (Jha et al., 2018).

Of course, microbiota changes were not the only pathway for animals undergoing domestication to respond to changing ecological factors. For example, genetic changes have enhanced the capacity for starch digestion in dogs (Axelsson et al., 2013; Reiter et al., 2016). Nevertheless, the increased microbial diversity and shifts in microbial composition that we observed in dogs may have additionally contributed to carbohydrate digestion. Indeed, dogs fed conventional diets have greater representation of carbohydrate metabolism genes in their gut metagenomes than do dogs fed meat-based diets (Alessandri et al., 2019). Notably, the microbiota has been found to supplement evolutionary responses during dietary niche expansion in wild animals that consume plants high in toxins (Kohl et al., 2014). As such, although hosts and their various gut microbial taxa are each expected to pursue their own fitness interests, gut microbial disparities observed between domesticated and wild animals, and more generally in other organisms under rapid environmental change, could potentially be adaptive for the host (Alberdi et al., 2016).

Beyond host support of a gut microbiota that can better digest a domesticate diet, humans may have selected for animals harboring a microbiota that helped them grow and reproduce well on such diets, thereby applying unconscious selection on the microbiota (Zohary et al., 1998). Changes in microbial function that enhanced host dietary energy harvest, survivorship, or reproduction may have been particularly important early in domestication, before host evolution occurred, although that hypothesis remains to be tested empirically. Regardless, specialization of microbial performance on domesticate diets could conceivably have come at the cost of broader digestive capacity, as seen in the laboratory mouse microbiota, which was better at harvesting energy from domesticate diets than from wild diets (Figure 2—figure supplement 2). It may also have impacted the immunological functions of the gut microbiota. The elevated pathogen abundances found in wild populations overall may largely be ascribed to low pathogen abundances in laboratory animals (Figure 1—figure supplement 2), which are maintained under specific pathogen-free conditions that minimize the likelihood of infection. Under natural conditions, though, the domesticated microbiota may exhibit reduced colonization resistance or immune system functioning (Rosshart et al., 2017; Beura et al., 2016; Rosshart et al., 2019), resulting in higher pathogen colonization, as observed here in agricultural animals. Future studies examining the trade-offs among microbially mediated functions, like digestive capacity, reproduction, and immunity, will help to illuminate the complex selection pressures shaping domesticated animals and their gut microbiota (Reese and Kearney, 2019).

We observed some correspondence between the gut microbial signatures of animal domestication and human industrialization that is most likely attributable to convergent ecological changes. The observation that gut microbial divergence among Pan and Homo primarily affects industrialized populations specifically implicates recent ecological changes as opposed to either ecological changes with deeper roots in human evolution or host evolutionary changes. Many recent human ecological changes involve accelerations of basic patterns established during the evolution of Homo, including increased proportion of calories from fat and protein, increased dependence on animal source foods, and extensive food processing involving both chemical and physical changes to food (Carmody, 2017). Other ecological changes are likely specific to industrialization, including reduced physical activity, high population density, and antibiotic use. These factors would be absent even in populations currently transitioning from subsistence to industrialized lifestyles (Jha et al., 2018), but may overlap with changes experienced by domesticated animals in their diets, habitats, and social milieu. While we limited our analysis to human–chimpanzee comparisons because Pan is the closest sister clade to Homo, recent work has indicated that the human gut microbiota is more similar to that of baboons (Gomez et al., 2019; Amato et al., 2019). Baboons are more distantly related to humans but have been argued to be closer in terms of diet and dietary physiology (Codron et al., 2008; Lambert, 1998), accentuating our finding of the importance of ecological factors in shaping the microbiota. Further work will be required to assess the specific combination of ecological factors driving similarities between domesticated and industrialized gut microbial signatures.

Because laboratory animals demonstrate some of the largest overall differences relative to their wild counterparts, they might be expected to have high translational potential as models for studying the gut microbiota of industrialized human populations. However, recent findings show that laboratory mice are poorer immunological models for humans in industrialized settings than are wild mice or laboratory mice harboring a wild microbiota (Beura et al., 2016; Rosshart et al., 2019). While the industrialized human gut microbiota exhibits parallels to those of domesticated animals, it may experience a broader array of environments and greater temporal variability; for example, greater ecological variability may explain the elevated gut microbial Shannon diversity seen in humans as compared to laboratory animals (Figure 1—figure supplement 2). Alternatively, it may be that domesticated laboratory animals are strong models for some aspects of host–microbe biology other than immunology. Certainly, studies of non-domesticated animals will be necessary to understand the natural history of host–microbe interactions (Reese and Kearney, 2019; Hird, 2017), as well as to determine the most appropriate models for translational research.

The fact that laboratory mice were permissive of recolonization by wild strains indicates that the local extinctions that occurred during domestication and/or generations in captivity can potentially be mitigated, thereby potentially improving the utility of these animals for research. Previous work has relied on laboratory mice colonized with a wild microbiota but fed standard laboratory chow (Rosshart et al., 2017; Rosshart et al., 2019) or on wild mice fed wild diets (Martínez-Mota et al., 2020). A combination of these approaches – adding wild gut microbial community members and feeding wild diet – would be expected to best support a wild gut microbiota in laboratory mice. A wild-microbiota laboratory-genotype model could be especially useful for studying infection challenges, disentangling host gene versus microbiota contributions to disease phenotypes, and testing for host–microbiota coevolution (Rosshart et al., 2019).

More generally, our data add to growing evidence that the gut microbiota is finely tuned to variations in the environment, affording at once expanded opportunities for biological mismatch to arise between the host and microbiota and for rapid microbiota-mediated host adaptation to novel environments. Further work to characterize the ecological significance of gut microbial plasticity will help reveal the fundamental nature of the host–microbial relationship, the conditions under which plasticity is beneficial versus detrimental, and the ecological conditions promoting cooperative, commensal, and competitive dynamics. The answers will have profound implications for our definition and pursuit of a healthy gut microbiome.

All sequencing data included in this study are available in the European Nucleotide Archive under accession number PRJEB36262.

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Author details

1. Aspen T Reese

   1. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, United States
   2. Society of Fellows, Harvard University, Cambridge, MA, United States

   Present address

   Ecology Behavior & Evolution Section, University of California San Diego, La Jolla, United States

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   areese@ucsd.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9004-9470

2. Katia S Chadaideh

   Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, United States

   Contribution

   Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2251-1170

3. Caroline E Diggins

   Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, United States

   Contribution

   Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

4. Laura D Schell

   Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, United States

   Contribution

   Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9600-924X

5. Mark Beckel

   Wildlife Science Center, Stacy, MN, United States

   Contribution

   Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

6. Peggy Callahan

   Wildlife Science Center, Stacy, MN, United States

   Contribution

   Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

7. Roberta Ryan

   Wildlife Science Center, Stacy, MN, United States

   Contribution

   Investigation, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

8. Melissa Emery Thompson

   Department of Anthropology, University of New Mexico, Albuquerque, NM, United States

   Contribution

   Funding acquisition, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

9. Rachel N Carmody

   Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, United States

   Contribution

   Conceptualization, Supervision, Funding acquisition, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   carmody@fas.harvard.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7505-9646

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