scholarly journals Roles of the gut microbiota in the adaptive evolution of mammalian species

2020 ◽  
Vol 375 (1808) ◽  
pp. 20190597 ◽  
Author(s):  
Andrew H. Moeller ◽  
Jon G. Sanders

Every mammalian species harbours a gut microbiota, and variation in the gut microbiota within mammalian species can have profound effects on host phenotypes. In this review, we summarize recent evidence that gut microbiotas have influenced the course of mammalian adaptation and diversification. Associations with gut microbiotas have: (i) promoted the diversification of mammalian species by enabling dietary transitions onto difficult-to-digest carbon sources and toxic food items; (ii) shaped the evolution of adaptive phenotypic plasticity in mammalian species through the amplification of signals from the external environment and from postnatal developmental processes; and (iii) generated selection for host mechanisms, including innate and adaptive immune mechanisms, to control the gut microbiota for the benefit of host fitness. The stability of specific gut microbiotas within host species lineages varies substantially across the mammalian phylogeny, and this variation may alter the ultimate evolutionary outcomes of relationships with gut microbiotas in different mammalian clades. In some mammalian species, including humans, relationships with host species-specific gut microbiotas appear to have led to the evolution of host dependence on the gut microbiota for certain functions. These studies implicate the gut microbiota as a significant environmental factor and selective agent shaping the adaptive evolution of mammalian diet, phenotypic plasticity, gastrointestinal morphology and immunity. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

2021 ◽  
Author(s):  
Jennifer L. Houtz ◽  
Jon G. Sanders ◽  
Anthony Denice ◽  
Andrew H. Moeller

2020 ◽  
Author(s):  
Connie A. Rojas ◽  
Santiago A. Ramírez-Barahona ◽  
Kay E. Holekamp ◽  
Kevin. R. Theis

AbstractThe gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host dietary guild in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders. We found that gut microbiotas were highly species-specific, and that host family accounted for more variation in the gut microbiota (35%) than did host dietary guild (14%). Overall, similarity among gut microbiotas increased with host phylogenetic relatedness (r=0.73), yet this relationship was not apparent among seven closely related Bovid host species (r=0.21 NS). In bovids, host dietary guild explained twice as much variation in the gut microbiota as did host species. Lastly, we found that the gut microbiotas of herbivores residing in southwest Kenya closely resemble those of conspecifics from central Kenya, suggesting that regardless of variability in host local habitat, hosts consistently provide microbes with similar niches for colonization. Overall, our findings suggest that host phylogeny may structure the gut microbiota at broad taxonomic scales, but that host ecology may be more influential in shaping the gut microbiotas of closely related host species.


Author(s):  
Jennifer Houtz ◽  
Jon Sanders ◽  
Anthony Denice ◽  
Andrew Moeller

Humans and non-human primates (NHPs) harbor complex gut microbial communities that affect phenotypes and fitness. The gut microbiotas of wild NHPs reflect their hosts’ phylogenetic histories and are compositionally distinct from those of humans, but in captivity the endogenous gut microbial lineages of NHPs can be lost or replaced by lineages found in humans. Despite its potential contributions to gastrointestinal dysfunction, this humanization of the gut microbiota has not been investigated systematically across captive NHP species. Here we show through comparisons of well-sampled wild and captive populations of apes and monkeys that the fraction of the gut microbiota humanized by captivity varies significantly between NHP species but is remarkably reproducible between captive populations of the same NHP species. Conspecific captive populations displayed significantly greater than expected overlap in the sets of bacterial 16S rRNA gene variants that were differentially abundant between captivity and the wild. This overlap was evident even between captive populations residing on different continents but was never observed between heterospecific captive populations. In addition, we developed an approach incorporating human gut microbiota data to rank NHPs’ gut microbial clades based on the propensity of their lineages to be lost or replaced by lineages found in humans in captivity. Relatively few microbial genera displayed reproducible degrees of humanization in different captive host species, but most microbial genera were reproducibly humanized or retained from the wild in conspecific pairs of captive populations. These results demonstrate that the gut microbiotas of captive NHPs display predictable, host-species specific responses to captivity.


2021 ◽  
Vol 3 (1) ◽  
Author(s):  
Connie A. Rojas ◽  
Santiago Ramírez-Barahona ◽  
Kay E. Holekamp ◽  
Kevin R. Theis

AbstractThe gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host diet in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders and dietary data (% C4 grasses in diet) were compiled from previously published sources. We found that herbivore gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity in the gut microbiota increased with host phylogenetic relatedness (r = 0.74) across the 11 species of herbivores, but among 7 closely related Bovid species, dietary %C4 grass values more strongly predicted gut microbiota structure (r = 0.64). Additionally, within bovids, host dietary guild explained more of the variation in the gut microbiota (17%) than did host species (12%). Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota across broad host taxonomic scales, but these gut microbiotas can be further modified by host ecology (i.e., diet, geography), especially among closely related host species.


mSphere ◽  
2019 ◽  
Vol 4 (4) ◽  
Author(s):  
Andrew H. Moeller ◽  
João C. Gomes-Neto ◽  
Sara Mantz ◽  
Hatem Kittana ◽  
Rafael R. Segura Munoz ◽  
...  

ABSTRACT The gut microbial communities of mammals have codiversified with host species, and changes in the gut microbiota can have profound effects on host fitness. Therefore, the gut microbiota may drive adaptation in mammalian species, but this possibility is underexplored. Here, we show that the gut microbiota has codiversified with mice in the genus Mus over the past ∼6 million years, and we present experimental evidence that the gut microbiota has driven adaptive evolution of the house mouse, Mus musculus domesticus. Phylogenetic analyses of metagenome-assembled bacterial genomic sequences revealed that gut bacterial lineages have been retained within and diversified alongside Mus species over evolutionary time. Transplantation of gut microbiotas from various Mus species into germfree M. m. domesticus showed that foreign gut microbiotas slowed growth rate and upregulated macrophage inflammatory protein in hosts. These results suggest adaptation by M. m. domesticus to its gut microbiota since it diverged from other Mus species. IMPORTANCE The communities of bacteria that reside within mammalian guts are deeply integrated with their hosts, but the impact of this gut microbiota on mammalian evolution remains poorly understood. Experimental transplantation of the gut microbiota between mouse species revealed that foreign gut microbiotas lowered the host growth rate and upregulated the expression of an immunomodulating cytokine. In addition, foreign gut microbiotas increased host liver sizes and attenuated sex-specific differences in host muscle and fat content. These results suggest that the house mouse has adapted to its species-specific gut microbiota.


2021 ◽  
Vol 15 ◽  
Author(s):  
Dehuang Kong ◽  
Lidewij Schipper ◽  
Gertjan van Dijk

Accumulating evidence implicates gut-microbiota-derived metabolites as important regulators of host energy balance and fuel homeostasis, the underlying mechanisms are currently subject to intense research. In this review, the most important executors, short chain fatty acids, which both directly and indirectly fulfill the interactions between gut microbiota and host will be discussed. Distinct roles of individual short chain fatty acids and the different effects they exert on host metabolism have long been overlooked, which compromises the process of clarifying the sophisticated crosstalk between gut microbiota and its host. Moreover, recent findings suggest that exogenously administered short chain fatty acids affect host metabolism via different mechanisms depending on the routes they enter the host. Although these exogenous routes are often artificial, they may help to comprehend the roles of the short-chain-fatty-acid mechanisms and signaling sites, that would normally occur after intestinal absorption of short chain fatty acids. Cautions should be addressed of generalizing findings, since different results have appeared in different host species, which may imply a host species-specific response to short chain fatty acids.


2020 ◽  
Author(s):  
Uswa Shahzad ◽  
Michael S Taccone ◽  
Sachin A Kumar ◽  
Hidehiro Okura ◽  
Stacey Krumholtz ◽  
...  

Abstract For decades, cell biologists and cancer researchers have taken advantage of non-murine species to increase our understanding of the molecular processes that drive normal cell and tissue development, and when perturbed, cause cancer. The advent of whole genome sequencing has revealed the high genetic homology of these organisms to humans. Seminal studies in non-murine organisms such as D. melanogaster, C. elegans, and D. rerio identified many of the signaling pathways involved in cancer. Studies in these organisms offer distinct advantages over mammalian cell or murine systems. Compared to murine models, these three species have shorter lifespans, are less resource intense, and are amenable to high-throughput drug and RNA interference screening to test a myriad of promising drugs against novel targets. In this review, we introduce species specific breeding strategies, highlight the advantages of modeling brain tumours in each non-mammalian species, and underscore the successes attributed to scientific investigation using these models. We conclude with an optimistic proposal that discoveries in the fields of cancer research, and in particular neuro-oncology, may be expedited using these powerful screening tools and strategies.


2021 ◽  
Vol 14 (8) ◽  
pp. 733
Author(s):  
Julia Aresti-Sanz ◽  
Markus Schwalbe ◽  
Rob Rodrigues Pereira ◽  
Hjalmar Permentier ◽  
Sahar El Aidy

Methylphenidate is one of the most widely used oral treatments for attention-deficit/hyperactivity disorder (ADHD). The drug is mainly absorbed in the small intestine and has low bioavailability. Accordingly, a high interindividual variability in terms of response to the treatment is known among ADHD patients treated with methylphenidate. Nonetheless, very little is known about the factors that influence the drug’s absorption and bioavailability. Gut microbiota has been shown to reduce the bioavailability of a wide variety of orally administered drugs. Here, we tested the ability of small intestinal bacteria to metabolize methylphenidate. In silico analysis identified several small intestinal bacteria to harbor homologues of the human carboxylesterase 1 enzyme responsible for the hydrolysis of methylphenidate in the liver into the inactive form, ritalinic acid. Despite our initial results hinting towards possible bacterial hydrolysis of the drug, up to 60% of methylphenidate is spontaneously hydrolyzed in the absence of bacteria and this hydrolysis is pH-dependent. Overall, our results indicate that the stability of methylphenidate is compromised under certain pH conditions in the presence or absence of gut microbiota.


1995 ◽  
Vol 73 (11) ◽  
pp. 1810-1823 ◽  
Author(s):  
Nicole S. Ramesar-Fortner ◽  
Nancy G. Dengler ◽  
Susan G. Aiken

Leaf phenotypic plasticity of 12 morphological, anatomical, and growth traits was investigated using four species of arctic Festuca (F. baffinensis, F. brachyphylla, F. edlundiae, and F. hyperborea). Plants collected around 78°N in the Canadian Arctic Archipelago were grown for 10 weeks at the University of Toronto in growth chambers in continuous light, under four regimes of temperature and moisture. Significant differences were found between leaves at the time of field collection and leaves of the same plant at the end of the experiment in (i) leaf blade length, (ii) surface vestiture, both in trichome density and angle of the trichomes to the blade surface, and (iii) characters seen in leaf cross sections: blade width, rib thickness, and inter-rib thickness. The four species responded similarly to the experimental conditions, indicating that most of these changes represent part of the developmentally inevitable component of plasticity rather than species-specific adaptations. Trichome density was the only characteristic for which species showed different patterns of response, with a unique pattern of response in F. edlundiae. This and certain growth traits support the taxonomic status of this newly recognized species. The significant effects of temperature and to a lesser degree, water treatments on these leaf anatomical traits indicate that they should be used with caution for the purposes of taxonomy and identification. Key words: Festuca, leaf blade anatomy, phenotypic plasticity.


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