Co-evolution in context: The importance of studying gut microbiomes in wild animals
22 Oct 2013-Vol. 1, Iss: 1, pp 10-29
TL;DR: Current knowledge of host-gut microbe dynamics is used to explore the potential interactions between host and microbe in natural habitats and the influence of host habitat on gut microbial community composition as well as the impacts of the gut microbiota on host fitness in a given habitat.
Abstract: Because the gut microbiota contributes to host nutrition, health and behavior, and gut microbial community composition differs according to host phylogeny, co-evolution is believed to have been an important mechanism in the formation of the host-gut microbe relationship. However, current research is not ideal for examining this theme. Most studies of the gut microbiota are performed in controlled settings, but gut microbial community composition is strongly influenced by environmental factors. To truly explore the co-evolution of host and microbe, it is necessary to have data describing host-microbe dynamics in natural environments with variation in factors such as climate, food availability, disease prevalence, and host behavior. In this review, I use current knowledge of host-gut microbe dynamics to explore the potential interactions between host and microbe in natural habitats. These interactions include the influence of host habitat on gut microbial community composition as well as the impacts of the gut microbiota on host fitness in a given habitat. Based on what we currently know, the potential connections between host habitat, the gut microbiota, and host fitness are great. Studies of wild animals will be an essential next step to test these connections and to advance our understanding of host-gut microbe co-evolution.
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TL;DR: Examining guano (feces) and distal intestinal mucosa from 19 species of free-ranging bats from Lamanai, Belize using 16S rRNA amplicon sequencing to compare microbial communities across sample types found that the diversity and composition of intestine and guano samples differed substantially.
Abstract: The gut microbiome is a community of host-associated symbiotic microbes that fulfills multiple key roles in host metabolism, immune function, and tissue development. Given the ability of the microbiome to impact host fitness, there is increasing interest in studying the microbiome of wild animals to better understand these communities in the context of host ecology and evolution. Human microbiome research protocols are well established, but wildlife microbiome research is still a developing field. Currently, there is no standardized set of best practices guiding the collection of microbiome samples from wildlife. Gut microflora are typically sampled either by fecal collection, rectal swabbing, or by destructively sampling the intestinal contents of the host animal. Studies rarely include more than one sampling technique and no comparison of these methods currently exists for a wild mammal. Although some studies have hypothesized that the fecal microbiome is a nested subset of the intestinal microbiome, this hypothesis has not been formally tested. To address these issues, we examined guano (feces) and distal intestinal mucosa from 19 species of free-ranging bats from Lamanai, Belize, using 16S rRNA amplicon sequencing to compare microbial communities across sample types. We found that the diversity and composition of intestine and guano samples differed substantially. In addition, we conclude that signatures of host evolution are retained by studying gut microbiomes based on mucosal tissue samples, but not fecal samples. Conversely, fecal samples retained more signal of host diet than intestinal samples. These results suggest that fecal and intestinal sampling methods are not interchangeable, and that these two microbiotas record different information about the host from which they are isolated.
333 citations
Cites background from "Co-evolution in context: The import..."
...…goal for evolutionary biology, ecology, and conservation Frontiers in Microbiology | www.frontiersin.org 7 May 2018 | Volume 9 | Article 803 (Amato, 2013; Hird, 2017; Kohl, 2017), but the study of microbiomes is complicated by numerous sources of bias that can impact any step of the…...
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...While most microbiome research has focused on humans and model organisms, microbiome studies in wildlife have recently gained popularity in light of the potential power of the microbiome to shape host evolution and ecology (e.g., Ley et al., 2008; Amato, 2013; Hird, 2017)....
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...Many studies of wild mammal microbiomes have sampled feces as a proxy for the gut microbiome (Schwab et al., 2009; Amato, 2013; Amato et al., 2014; Kohl et al., 2015; Menke et al., 2015; Phillips et al., 2017)....
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TL;DR: The state of microbiome studies of nonmammalian vertebrates are reviewed and a synthesis of emerging patterns in the microbiome of those organisms is provided, highlighting the importance of collection methods, and the need for greater taxonomic sampling of natural rather than captive hosts.
Abstract: Vertebrates harbour microbes both internally and externally, and collectively, these microorganisms (the 'microbiome') contain genes that outnumber the host's genetic information 10-fold. The majority of the microorganisms associated with vertebrates are found within the gut, where they influence host physiology, immunity and development. The development of next-generation sequencing has led to a surge in effort to characterize the microbiomes of various vertebrate hosts, a necessary first step to determine the functional role these communities play in host evolution or ecology. This shift away from a culture-based microbiological approach, limited in taxonomic breadth, has resulted in the emergence of patterns suggesting a core vertebrate microbiome dominated by members of the bacterial phyla Bacteroidetes, Proteobacteria and Firmicutes. Still, there is a substantial variation in the methodology used to characterize the microbiome, from differences in sample type to issues of sampling captive or wild hosts, and the majority (>90%) of studies have characterized the microbiome of mammals, which represent just 8% of described vertebrate species. Here, we review the state of microbiome studies of nonmammalian vertebrates and provide a synthesis of emerging patterns in the microbiome of those organisms. We highlight the importance of collection methods, and the need for greater taxonomic sampling of natural rather than captive hosts, a shift in approach that is needed to draw ecologically and evolutionarily relevant inferences. Finally, we recommend future directions for vertebrate microbiome research, so that attempts can be made to determine the role that microbial communities play in vertebrate biology and evolution.
280 citations
Cites background from "Co-evolution in context: The import..."
...This problem has been suggested before (Amato 2013), yet there is still a substantial lack of studies that have attempted to characterize the enteric microbial communities in hosts within a natural environment (Tables 1 and S1, Supporting information)....
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TL;DR: This review calls for the microbial renaissance of conservation biology, where biodiversity of host-associated microbiota is recognized as an essential component of wildlife management practices and integrates approaches for maintaining microbial diversity to successfully achieve conservation objectives.
Abstract: The central aim of conservation biology is to understand and mitigate the effects of human activities on biodiversity. To successfully achieve this objective, researchers must take an interdiscipli...
227 citations
TL;DR: In this paper, a perspective article collates important microbiome research in threatened animals from around the world to make a case for the inclusion of microbial research in modern conservation practice, which is often impeded by poor animal health and low reproductive success.
161 citations
TL;DR: How chronically exposed species may suffer from microplastics-induced gut dysbiosis, deteriorating host health, and corresponding future directions of research are summarized.
159 citations
References
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TL;DR: It is demonstrated through metagenomic and biochemical analyses that changes in the relative abundance of the Bacteroidetes and Firmicutes affect the metabolic potential of the mouse gut microbiota and indicates that the obese microbiome has an increased capacity to harvest energy from the diet.
Abstract: The worldwide obesity epidemic is stimulating efforts to identify host and environmental factors that affect energy balance. Comparisons of the distal gut microbiota of genetically obese mice and their lean littermates, as well as those of obese and lean human volunteers have revealed that obesity is associated with changes in the relative abundance of the two dominant bacterial divisions, the Bacteroidetes and the Firmicutes. Here we demonstrate through metagenomic and biochemical analyses that these changes affect the metabolic potential of the mouse gut microbiota. Our results indicate that the obese microbiome has an increased capacity to harvest energy from the diet. Furthermore, this trait is transmissible: colonization of germ-free mice with an 'obese microbiota' results in a significantly greater increase in total body fat than colonization with a 'lean microbiota'. These results identify the gut microbiota as an additional contributing factor to the pathophysiology of obesity.
10,126 citations
TL;DR: It is shown that the relative proportion of Bacteroidetes is decreased in obese people by comparison with lean people, and that this proportion increases with weight loss on two types of low-calorie diet.
Abstract: Two groups of beneficial bacteria are dominant in the human gut, the Bacteroidetes and the Firmicutes. Here we show that the relative proportion of Bacteroidetes is decreased in obese people by comparison with lean people, and that this proportion increases with weight loss on two types of low-calorie diet. Our findings indicate that obesity has a microbial component, which might have potential therapeutic implications.
7,550 citations
Book•
03 Sep 2009
TL;DR: The "Penguin Classics" edition of "On the Origin of Species" as discussed by the authors contains an introduction and notes by William Bynum, and features a cover designed by Damien Hirst.
Abstract: Charles Darwin's seminal formulation of the theory of evolution, "On the Origin of Species" continues to be as controversial today as when it was first published. This "Penguin Classics" edition contains an introduction and notes by William Bynum, and features a cover designed by Damien Hirst. Written for a general readership, "On the Origin of Species" sold out on the day of its publication and has remained in print ever since. Instantly and persistently controversial, the concept of natural selection transformed scientific analysis about all life on Earth. Before the "Origin of Species", accepted thinking held that life was the static and perfect creation of God. By a single, systematic argument Darwin called this view into question. His ideas have affected public perception of everything from religion to economics. William Bynum's introduction discusses Darwin's life, the publication and reception of the themes of "On the Origin of Species", and the subsequent development of its major themes. The new edition also includes brief biographies of some of the most important scientific thinkers leading up to and surrounding the "Origin of Species", suggested further reading, notes and a chronology. Charles Darwin (1809-82), a Victorian scientist and naturalist, has become one of the most famous figures of science to date. The advent of "On the Origin of Species" by means of natural selection in 1859 challenged and contradicted all contemporary biological and religious beliefs. If you enjoyed "On the Origin of Species", you might like Darwin's "The Descent of Man", also available in "Penguin Classics".
7,487 citations
TL;DR: The faecal microbial communities of adult female monozygotic and dizygotic twin pairs concordant for leanness or obesity, and their mothers are characterized to address how host genotype, environmental exposure and host adiposity influence the gut microbiome.
Abstract: The human distal gut harbours a vast ensemble of microbes (the microbiota) that provide important metabolic capabilities, including the ability to extract energy from otherwise indigestible dietary polysaccharides. Studies of a few unrelated, healthy adults have revealed substantial diversity in their gut communities, as measured by sequencing 16S rRNA genes, yet how this diversity relates to function and to the rest of the genes in the collective genomes of the microbiota (the gut microbiome) remains obscure. Studies of lean and obese mice suggest that the gut microbiota affects energy balance by influencing the efficiency of calorie harvest from the diet, and how this harvested energy is used and stored. Here we characterize the faecal microbial communities of adult female monozygotic and dizygotic twin pairs concordant for leanness or obesity, and their mothers, to address how host genotype, environmental exposure and host adiposity influence the gut microbiome. Analysis of 154 individuals yielded 9,920 near full-length and 1,937,461 partial bacterial 16S rRNA sequences, plus 2.14 gigabases from their microbiomes. The results reveal that the human gut microbiome is shared among family members, but that each person's gut microbial community varies in the specific bacterial lineages present, with a comparable degree of co-variation between adult monozygotic and dizygotic twin pairs. However, there was a wide array of shared microbial genes among sampled individuals, comprising an extensive, identifiable 'core microbiome' at the gene, rather than at the organismal lineage, level. Obesity is associated with phylum-level changes in the microbiota, reduced bacterial diversity and altered representation of bacterial genes and metabolic pathways. These results demonstrate that a diversity of organismal assemblages can nonetheless yield a core microbiome at a functional level, and that deviations from this core are associated with different physiological states (obese compared with lean).
6,970 citations
TL;DR: In this article, the authors suggest that the term "fragmentation" should be reserved for the breaking apart of habitat, independent of habitat loss, and that fragmentation per se has much weaker effects on biodiversity that are at least as likely to be positive as negative.
Abstract: ■ Abstract The literature on effects of habitat fragmentation on biodiversity is huge. It is also very diverse, with different authors measuring fragmentation in different ways and, as a consequence, drawing different conclusions regarding both the magnitude and direction of its effects. Habitat fragmentation is usually defined as a landscape-scale process involving both habitat loss and the breaking apart of habitat. Results of empirical studies of habitat fragmentation are often difficult to interpret because (a) many researchers measure fragmentation at the patch scale, not the landscape scale and (b) most researchers measure fragmentation in ways that do not distinguish between habitat loss and habitat fragmentation per se, i.e., the breaking apart of habitat after controlling for habitat loss. Empirical studies to date suggest that habitat loss has large, consistently negative effects on biodiversity. Habitat fragmentation per se has much weaker effects on biodiversity that are at least as likely to be positive as negative. Therefore, to correctly interpret the influence of habitat fragmentation on biodiversity, the effects of these two components of fragmentation must be measured independently. More studies of the independent effects of habitat loss and fragmentation per se are needed to determine the factors that lead to positive versus negative effects of fragmentation per se. I suggest that the term “fragmentation” should be reserved for the breaking apart of habitat, independent of habitat loss.
6,341 citations