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Conservation Genetics

, Volume 20, Issue 1, pp 19–27 | Cite as

Conserve the germs: the gut microbiota and adaptive potential

  • Heidi C. HauffeEmail author
  • Claudia Barelli
Open Access
Perspective

Abstract

Although the diversity of microbial communities (microbiota) inhabiting body niches are of proven importance to health in both humans and non-human animals, the functional importance of these collective genomes (microbiome) to the adaptive potential of their hosts has only recently been considered within a conservation framework. If loss of gut biodiversity threatens the health (and therefore the fitness of individuals), and this loss can be correlated with the adaptive potential of a species in changing environments, measuring functional composition of the microbiota from non-invasive samples, such as faeces and skin swabs, could provide a useful and practical tool for determining conservation priorities. This article reviews the evidence for adaptive potential of microbiota in wild species, and proposes future directions. While there is ample indication of inter- and intra-specific variation in microbiota diversity, there is little evidence that diversity per se confers fitness. However, there are convincing examples showing that microbiota flexibility, composition and function may well be sources of adaptive potential, although case studies are relatively few, and the analytical approaches needed to demonstrate the mechanisms underlying host–microbiota interactions have only recently been developed.

Keywords

Conservation Fitness Host health Metataxonomics Microbiodiversity Microbiome 

As this volume explores in depth, in conservation genetics, attention has turned from the near-exclusive use of neutral genetic variation, to the more challenging prospect of estimating adaptive genetic variation, essential for the survival of endangered organisms, especially in rapidly changing environments. Such progress in our understanding is thanks to advancements in next generation sequencing (NGS), allowing markers to be characterized across the genome or even whole genomes to be sequenced. Even more recently, NGS technology has allowed the characterization of whole communities of microorganisms from various sample types using taxa-specific markers (‘metataxonomics’; Marchesi and Ravel 2015), with rapid parallel development of appropriate field collection methods (Hale et al. 2016; Song et al. 2016) and bioinformatic analyses (e.g. Callahan et al. 2017; Jiménez and Sommer 2017; Mendes et al. 2017).

It has been recognized that the bacteria inhabiting body niches (e.g. skin, gut) of wild animals may be important to maintaining individual health and resilience as has been shown extensively for humans, laboratory models and livestock (Cho and Blaser 2012; Pascoe et al. 2017). While the conservation implications of an intact microbiota have started to be explored (e.g. Roggenbuck et al. 2014; Stumpf et al. 2016; Jiménez and Sommer 2017; West et al. 2019), fewer than 100 article titles, abstracts and/or keywords contain both ‘microbiota’ and ‘conservation’ in a literature search of public databases. In addition, evaluation of available literature on wildlife microbiota reveals that most articles are dedicated to simply cataloguing the composition of these bacterial communities (Pascoe et al. 2017). Thus, whether microbiota influences the adaptive potential of wild species has rarely been specifically addressed up to now (Bahrndorff et al. 2016). This review explores the evidence relevant to this potential, with the aim of establishing whether ‘microbiodiversity conservation’ should be considered concomitantly with conservation of host genomic variability to improve the management and survival of species at risk. Such evidence will mainly be derived from wild species, since these are more likely to possess intact microbiota demonstrating the natural relationships between host and commensal flora (e.g. Amato 2013; Pascoe et al. 2017). Since the majority of studies thus far have focussed on the effect of bacterial composition and not that of their collective genomes as such, this review will be limited to discussions of the microbiota, not the microbiome, as a source of adaptive potential.

The importance of commensal bacterial communities to host physiology, nutrition and immune health has resulted in some authors declaring that microbiota should be considered a new ‘organ’ (Baquero and Nombela 2012) or that all genomes of an individual, including that of the individual and the microbiome, should be considered as a single evolutionary unit, or ‘holobiome’ (Zilber-Rosenberg and Rosenberg 2008; Shapira 2016). However, given the complexity of the microbiota and the multiplicity of organisms that it encompasses (including symbiotic, commensal and potentially pathogenic organisms) other authors including ourselves consider this an unnecessary and possibly erroneous simplification, instead promoting the use of well-established ecological theory to analyse the relationships between the microbiota and host (Moran and Sloan 2015; Douglas and Werren 2016). In any case, relevant to the argument here is that microbiota has an effect on a host’s phenotype, and therefore, on fitness, affecting natural selection and evolutionary trajectory (Redford et al. 2012; Sharpton 2018). Essentially, in order for these bacterial communities to be a source of adaptive potential for their respective host species, intraspecific variation in microbiota composition and function must be (i) present; (ii) heritable, and (iii) have an effect on individual host fitness for natural selection to be able to act.

Does intra-specific variation in microbiota composition exist, and is it heritable?

There is a wealth of evidence to confirm that intra-specific variation in the microbiota of healthy adult individuals exists for the same body niche. For example, individual variation in gut microbiota composition has been noted in the gorilla Gorilla gorilla (Frey et al. 2006), chimpanzee Pan troglodytes (Degnan et al. 2012), koala Phascolarctos cinereus (Alfano et al. 2015) and kākāpō Strigops habroptilus (Waite et al. 2012), and in skin microbiota in the bottlenose dolphin Tursiops truncates, killer whale Orcinus orca (Chiarello et al. 2017), and several marine fish species (Chiarello et al. 2015). In addition, variation in gut microbiota composition between sexes has been noted for the black howler monkey Alouatta pigra (Amato et al. 2014), Verreaux’s sifaka Propithecus verreauxi (Springer et al. 2017), Namibian cheetah Acinonyx jubatus (Wasimuddin et al. 2017) and largemouth bronze gudgeon Coreius guichenoti (Li et al. 2016).

The heritability of microbiota is, by comparison, much less studied, especially in wildlife (but see review on humans by Koskella et al. 2017, including successful experimental approaches). Despite the complexity of these microbial communities, stable, measureable species-specific differences in composition are evident, suggesting that these may be ‘heritable’; that is, passed on to future generations by vertical transmission, and co-evolve with their hosts (Baldo et al. 2017). Phylogenetic analyses of the gut microbiota of humans and chimpanzees (Moeller et al. 2012), 59 mammals (Ley et al. 2008), eight species of lagomorphs and rodents (Li et al. 2017b), 25 Cephalotes ant species (Sanders et al. 2014), and Nasonia parasitoid wasps (Brucker and Bordenstein 2012) are consistent with evolutionary relationships estimated from host genomes. Specifically, Sanders et al. (2014) used an innovative analysis to show that vertical transmission was the most likely factor affecting microbiota stability of host-microbiota co-evolution. In addition, composition of the gut microbiota distinguishes host species, even when there is convergence in specialized diets and some microbial gut taxa, as is the case for bamboo-feeding (Li et al. 2015; McKenney et al. 2018), piscivorous (Soverini et al. 2016), 18 folivorous (Amato et al. 2018) and 15 myrmecophagous (Delsuc et al. 2014) mammals (but see Baldo et al. 2017 for cichlid fishes). Microbiota composition is also preserved across geographically separated populations, e.g. in tunicates (Cahill et al. 2016).

Does intra-specific variation in microbiota composition or diversity affect individual fitness?

Although core microbiota composition may be stable and heritable for a particular species, animal microbiota composition may also change within an individual in association with extrinsic and intrinsic factors. For example, as for humans and livestock, diet is a common driver of composition (Muegge et al. 2011; Pascoe et al. 2017), as illustrated by studies of the black howler monkey A. pigra (Amato et al. 2015), giant panda (Xue et al. 2015; Williams et al. 2016; Wu et al. 2017), Tasmanian devil Sarcophilus harrisii (Cheng et al. 2015), American bison Bison bison (Bergmann et al. 2015), American pika Ochotona princeps (Kohl et al. 2017), and birds (Waite and Taylor 2015; see also discussion of captive species below). Several authors have noted that habitat also appears to be a critical factor determining surface microbiota in corals (Kelly et al. 2014; Roder et al. 2015), plethodontid salamanders (Muletz Wolz et al. 2017) and various carp species (Eichmiller et al. 2016), as well as the gut microbiota of the Namibian black­backed jackal Canis mesomelas (Menke et al. 2017) and ring-tailed lemurs Lemur catta (Bennett et al. 2016). Other authors have noted differences in microbiota diversity and composition for various life stages suggesting that early exposure to many sources of microbiota could have important consequences for host health later in life (e.g. howler monkeys: Amato et al. 2014; kittiwakes: Van Dongen et al. 2013; 212 amphibians: Vences et al. 2016; bees: McFrederick et al. 2014), as has been demonstrated in humans (Odamaki et al. 2016). The fact that changes in microbiota composition are associated with available food and other resources suggests that microbiota flexibility may affect an individual’s resilience to changes in the environment throughout its lifetime (including resistance to pathogens), and therefore, could impact individual health, survival and, consequently, fitness; in other words, such plasticity could act as an adaptive trait, as has been suggested for host phenotypes (Fusco and Minelli 2010). However, the causes and effects of specific changes in taxa have rarely been verified. Only a few very careful studies thus far have come close. Kohl et al. (2017) have shown that the gut microbiota of the American pika is particularly well-adapted to their specialized moss diet, being enriched with fibre-degrading Melainabacteria. Sommer et al. (2016) noted changes in microbiota composition in the brown bear Ursus arctos during active and hibernation seasons and investigated further: by transplanting specific summer and winter microbiota from bear to germ-free laboratory mice, Sommer and colleagues were able to show that changes in gut microbiota composition were directly related to fat accumulation and metabolism, both related to individual fitness.

From human studies, we know that low bacterial diversity is associated with ‘western’ diets (De Filippo et al. 2010), and dysbiosis with bowel disease (Gonçalves et al. 2018 and references therein), but also other health issues (e.g. Battson et al. 2017 for cardiovascular disease; Moran-Ramos et al. 2017 for metabolic disease). Therefore, if microbiota diversity affects individual fitness, low microbiota diversity resulting in microbiota dysfunction would be expected in circumstances where adaptive capacity is compromised. For wild species, such circumstances might be predicted in captivity, where individuals are often fed high energy or other inappropriate diets, are highly stressed and/or have little contact with natural environments (which provide a reservoir of taxa from which host microbiota are normally maintained). Microbiota studies on captive and wild populations provide some evidence that microbiota diversity decreases in captivity, but the pattern is not straightforward. In a recent review on wild versus captive mammalian microbiota, McKenzie et al. (2017) concluded that many primates, canids, and equids have a lower gut microbiota alpha diversity in captivity than in the wild. Carnivorous marsupials such as the Tasmanian devil also suffer a decrease in microbiota alpha diversity in captivity (Cheng et al. 2015), as do the mainly herbivorous Andean bear Tremarctos ornatus (Borbón-García et al. 2017) and red panda Ailurus fulgens (Kong et al. 2014), and piscivorous Yangze finless porpoise Neophocaena asiaeorientalis asiaeorientalis (Wan et al. 2016). However, many other herbivores and myrmecophagous mammals show no changes to their microbiota in captivity. Perhaps surprisingly, given their apparent sensitivity, some frog species also appear to maintain their natural skin microbiota diversity in captivity (Flechas et al. 2017), but not all (see Antwis et al. 2014 for red-eyed tree frog Agalychnis callidryas). Other species even show an increase in microbiota diversity in captivity, including rhinoceros (see McKenzie et al. 2017), and some birds (red-crowned crane Grus japonensis; Xie et al. 2016). Based on studies of rodents, Kohl et al. (2014) concluded that specialist feeders may be more sensitive to captive conditions, but this does not always appear to be the case (e.g. myrmecophagous mammals, mentioned above). Occasionally, a loss of diversity has been linked directly to a specific component lacking in the diet of captive individuals (such as carotenoids for frogs; Antwis et al. 2014); however, in most studies diet does not appear to be the only factor affecting changes in microbiota diversity, but a more complex combination of diet, phylogeny, and living conditions. Several recent studies suggest that it may be informative to look for potential impacts of captivity on gut health in microbiota composition, rather than simply measuring diversity; for example, in the microbiota’s capacity to resist pathogen invasion. For example, the Namibian cheetah shows no change in diversity between captive and wild conditions, but captive animals have a higher abundance of potentially pathogenic micro-organisms in their gut microbiota (Wasimuddin et al. 2017); a similar pattern is reported for captive versus wild forest musk deer Moschus berezovskii (Hu et al. 2017; Li et al. 2017a), rock ptarmigan (Ushida et al. 2016), swan geese Anser cygnoides (Wang et al. 2016) and crocodile lizards Shinisaurus crocodilurus (Jiang et al. 2017).

If microbiota diversity is associated with species survival, we might also expect that endangered species to have low diversity if they are at a particularly low population size, and/or are forced to survive in suboptimal habitats, such as those that are highly fragmented. Waite et al. (2012) has found an extremely low Phylum-level diversity in the critically endangered kākāpō compared to other species studied thus far, but even this example of low diversity may be related to its specialist leaf-chewing habit, not conservation status (Waite et al. 2012; Perry et al. 2017). Lower diversity has also been found in fragmented populations of several primate species compared to populations in intact habitat, those of the black howler monkey A. pigra (Amato et al. 2013) and Udzungwa red colobus Procolobus gordonorum (Barelli et al. 2015), but not in disturbed populations of primates in Uganda (McCord et al. 2014). However, more specifically, Amato et al. (2013) found that the gut microbiota of howler monkeys from intact habitats were composed of higher abundances of beneficial bacteria. Barelli et al. (2015) also reported that the lower diversity in gut microbiota in red colobus from fragmented habitats translated into a loss of microbiota function, i.e. loss of genomes conferring the ability to digest toxic plant compounds. Therefore, the effect of lower diversity on microbiota function appears to be more important than diversity alone. However, in both examples, direct evidence that this loss of diversity or function has a measureable effect on individual health or fitness still needs to be demonstrated.

Direct evidence for adaptive potential of microbiota

Does the microbiota provide adaptive potential in the long-term? In other words, does the co-evolution of the host-microbiota interaction affect host evolution? There is certainly some intriguing evidence that microbiota composition or diversity directly affects fitness. In their review, Lizé et al. (2013) brings together a number of examples of how microbiota could affect behaviour, but the most convincing case in point, providing the mechanism underlying the link, concerns the fruit fly Drosophila melanogaster: in this species, the gut microbiota has been shown to influence cuticular hydrocarbon profiles (sex pheromones), which determine individual scent, and therefore mate selection (Sharon et al. 2010). In another elegant study using a combination of metagenomics, transcriptomics and metabolomics, Vogel et al. (2017) show how each gut section of the burying beetle Nicrophorus vespilloides has a specialized microbiota with specific activity for digesting and detoxifying its ephemeral food sources, as well as providing oral and anal excretions that these beetles apply to carcasses to preserve this resource for its larvae.

For several wild species, microbiota has also been shown to confer an immune phenotype. For example, the survival of Panamanian golden frogs Atelopus zeteki infected with the chytrid fungus Batrachochytrium dendrobatidis is predicted by the composition of skin microbiota in this amphibian (Becker et al. 2015). Interestingly from a conservation standpoint, Becker et al. (2017) went on to show that such composition is maintained among populations by habitat corridors, ensuring interactions between individuals from different populations, while other authors are identifying the exact strains of bacteria responsible for the anti-fungal activity (Madison et al. 2017; Woodhams et al. 2017). Similarly, Lemieux-Labonté et al. (2017) reported that the skin microbiota of little brown bats Myotis lucifugus that survive infection of the fungus causing white-nose syndrome Pseudogymnoascus destructans, was less diverse than that of bats that did not survive, but had a higher prevalence of taxa known for their anti-fungal activity. The eggs of the sea turtle Eretmochelys imbricate have been shown to have a surface microbiota with taxa showing activity against the pathogen Fusarium falciforme (Sarmiento-Ramírez et al. 2014). Bumblebee Bombus terrestris gut microbiota also protects individuals from invasion of the intestinal parasite Crithidia bombi (although these were laboratory studies; Koch and Schmid-Hempel 2011) and similarly, the gut microbiota of Manila clams Ruditapes philippinarum includes detoxifying bacteria allowing them to cope with winter water pollution (Milan et al. 2018). Lastly, in a transplant experiment, Macke et al. (2017) showed how gut microbiota (in combination with genotype) protects the freshwater crustacean Daphnia magna from toxic cyanobacteria.

Conclusions and future directions in conservation

If microbiota confers adaptive potential, then loss of this potential could be an additional factor together with loss of genetic diversity and habitat loss leading to species extinction. Because the effects of microbiota loss, like loss of genetic biodiversity, may only become measurable at the host phenotypic or population level when loss is irreversible (e.g. gut dysbiosis leading to visibly ill individuals or negative population growth), it is important to consider the conservation implications of microbiodiversity loss along with other factors threatening specific species.

This review indicates that there is now intriguing evidence in wild animal species of an association between host genotype and microbiota composition (i.e. microbiota appears heritable), combined with extensive intraspecific variation in these bacterial communities, as shown in humans. Such variation confers flexibility and adaptive ability (e.g. to diet), and could certainly be useful to individuals in periods of very rapid climate change and habitat destruction during the host’s lifetime. The extent and functional significance of a flexibile microbiota diversity and composition within individuals may be considered an adaptive phenotype in itself, as suggested by the pika and bear examples above, with implications for host evolution and species survival (Erkosar et al. 2017); however, more examples are needed to demonstrate a pattern of causality, and show that flexibility itself is variable and heritable. The constraints on flexibility due to physiology and phylogeny also need to be better understood (e.g. Koskella et al. 2017; Amato et al. 2018). From a conservation point of view, better knowledge of the ‘intact’ diversity of microbiota in wild species of interest would also be useful for identifying which biotic or abiotic factors cause loss of diversity or function (e.g. Waite et al. 2012; Barelli et al. 2015; Stumpf et al. 2016), and possibly to facilitate the restoration of the original microbial diversity if this is deemed beneficial for species recovery in what Jiménez and Sommer (2017) term a ‘meta-organism conservation approach’ (Bahrndorff et al. 2016; see also attempts at enriching skin microbiota to combat pathogens, e.g. Küng et al. 2014, and review by Stumpf et al. 2016). The attraction of adding this potentially powerful tool to the conservation ‘omics repertoire has already inspired biologists to adopt creative and non-invasive methods of sample collection, such as using drones to collect whale blow for monitoring lung microbiota (Apprill et al. 2017).

Although an ‘unhealthy’ gut in humans has been associated with low bacterial diversity, there is little evidence from wild animals that diversity per se is associated with individual fitness, in both captive or endangered species. Instead, there are increasing indications that microbiota composition and function are more relevant, conferring, for example, immune phenotypes, the ability to detoxify food resources, behavioural traits, or resistance to pathogens, all of which are known to have direct effects on lifetime fitness. Although diversity level and microbiota composition will vary across species even with the same diet (see examples above), with data from more species, some patterns may become more evident, especially with regards function (e.g. generalist vs. specialist; common vs. rare). In fact, functional redundancy, or the ability of various bacterial compositions to provide the same function, needs to be explored, and may even provide the flexibility needed to overcome change, or evolutionary constraints, without loss of fitness (Sharpton 2018). Investigating microbiota function is still in its infancy even in human studies (Degli Esposti and Martinez Romero 2017; Moran-Ramos et al. 2017), but becoming more common even in wildlife with the advent of more powerful algorithms and adequate databases, and is essential to understanding the adaptive potential of the microbiota (Hernández-Gómez et al. 2017). Recent laboratory studies in mice using multi-‘omics data (metataxonomics, trascriptomics, proteomics) also show how it is possible to identify the exact mechanisms of microbiota function (Manes et al. 2017). Again, such comparative analyses are becoming possible thanks to the development of more sophisticated analytical tools (e.g. Callahan et al. 2017; Zhai et al. 2017). However, experimental work will also be essential to connect genotypes with phenotypes and their impacts on fitness, especially because so little is known about the function of the underlying metagenome or even how functions are defined, gained and lost.

At least one other aspect of microbiota ecology with respect to adaptive potential are also virtually unknown. Just as wildlife corridors are considered essential for maintaining or restoring exchange of individuals between isolated populations and, therefore gene flow, the routes of microbiota transmission between individuals and populations should be investigated and understood. However, at present, even in humans this process is virtually unexplored (Browne et al. 2017), although it has been suggested that transmission mode may be critical to the role of microbiota in host evolution (Rodrigo et al. 2017), as well as to microbiota-host co-evolution (Sanders et al. 2014).

Notes

Acknowledgements

The writing of this article has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant Agreement No. 752399 (WILDGUT).

References

  1. Alfano N, Courtiol A, Vielgrader H, Timms P, Roca AL, Greenwood AD (2015) Variation in koala microbiomes within and between individuals: effect of body region and captivity status. Sci Rep 5:10189.  https://doi.org/10.1038/srep10189 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amato KR (2013) Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci Med 1:10–29.  https://doi.org/10.2478/micsm-2013-0002 CrossRefGoogle Scholar
  3. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, Gaskins HR, Stumpf RM, Yildirim S, Torralba M, Gillis M, Wilson BA, Nelson KE, White BA, Leigh SR (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344–1353.  https://doi.org/10.1038/ismej.2013.16 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, Wilson BA, Nelson KE, White BA, Garber PA (2014) The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra). Am J Phys Anthropol 155:652–664.  https://doi.org/10.1002/ajpa.22621 CrossRefPubMedGoogle Scholar
  5. Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, Wilson BA, Nelson KE, White BA, Garber PA (2015) The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb Ecol 69:434–443.  https://doi.org/10.1007/s00248-014-0554-7 CrossRefPubMedGoogle Scholar
  6. Amato KR, Sanders JG, Song SJ, Nute M, Metcalf JL, Thompson LR, Morton JT, Amir A, McKenzie VJ, Humphrey G, Gogul G, Gaffney J, Baden AL, Britton GAO, Cuozzo FP, Di Fiore A, Dominy NJ, Goldberg TL, Gomez A, Kowalewski MM, Lewis RJ, Link A, Sauther ML, Tecot S, White BA, Nelson KE, Stumpf RM, Knight R, Leigh SR (2018) Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J.  https://doi.org/10.1038/s41396-018-0175-0 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Antwis RE, Haworth RL, Engelmoer DJ, Ogilvy V, Fidgett AL, Preziosi RF (2014) Ex situ diet influences the bacterial community associated with the skin of red-eyed tree frogs (Agalychnis callidryas). PLoS ONE 9:e85563.  https://doi.org/10.1371/journal.pone.0085563 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Apprill A, Miller CA, Moore MJ, Durban JW, Fearnbach H, Barrett-Lennard LG (2017) Extensive core microbiome in drone-captured whale blow supports a framework for health monitoring. mSystems 2:e00119-17.  https://doi.org/10.1128/mSystems.00119-17 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J (2016) The microbiome of animals: implications for conservation biology. Int J Genomics 2016:e5304028.  https://doi.org/10.1155/2016/5304028 CrossRefGoogle Scholar
  10. Baldo L, Pretus JL, Riera JL, Musilova Z, Bitja Nyom AR, Salzburger W (2017) Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes. ISME J 11:1975–1987.  https://doi.org/10.1038/ismej.2017.62 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Baquero F, Nombela C (2012) The microbiome as a human organ. Clin Microbiol Infect 18:2–4.  https://doi.org/10.1111/j.1469-0691.2012.03916.x CrossRefPubMedGoogle Scholar
  12. Barelli C, Albanese D, Donati C, Pindo M, Dallago C, Rovero F, Cavalieri D, Tuohy KM, Hauffe HC, DeFilippo C (2015) Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci Rep 5:14862.  https://doi.org/10.1038/srep14862 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Battson ML, Lee DM, Weir TL, Gentile CL (2017) The gut microbiota as a novel regulator of cardiovascular function and disease. J Nutr Biochem 56:1–15.  https://doi.org/10.1016/j.jnutbio.2017.12.010 CrossRefPubMedGoogle Scholar
  14. Becker MH, Walke JB, Cikanek S, Savage AE, Mattheus N, Santiago CN, Minbiole KPC, Harris RN, Belden LK, Gratwicke B (2015) Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proc R Soc B 282:20142881.  https://doi.org/10.1098/rspb.2014.2881 CrossRefPubMedGoogle Scholar
  15. Becker CG, Longo AV, Haddad CFB, Zamudio KR (2017) Land cover and forest connectivity alter the interactions among host, pathogen and skin microbiome. Proc Biol Sci 284:20170582.  https://doi.org/10.1098/rspb.2017.0582 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bennett G, Malone M, Sauther ML, Cuozzo FP, White B, Nelson KE, Stumpf RM, Knight R, Leigh SR, Amato KR (2016) Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta). Am J Primatol 78:883–892.  https://doi.org/10.1002/ajp.22555 CrossRefPubMedGoogle Scholar
  17. Bergmann GT, Craine JM, Robeson MS II, Fierer N (2015) Seasonal shifts in diet and gut microbiota of the American bison (Bison bison). PLoS ONE 10:e0142409.  https://doi.org/10.1371/journal.pone.0142409 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Borbón-García A, Reyes A, Vives-Flórez M, Caballero S (2017) Captivity shapes the gut microbiota of Andean bears: insights into health surveillance. Front Microbiol 8:1316.  https://doi.org/10.3389/fmicb.2017.01316 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Browne HP, Neville BA, Forster SC, Lawley TD (2017) Transmission of the gut microbiota: spreading of health. Nat Rev Microbiol 15:531–543.  https://doi.org/10.1038/nrmicro.2017.50 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Brucker RM, Bordenstein SR (2012) The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66:349–362.  https://doi.org/10.1111/j.1558-5646.2011.01454.x CrossRefPubMedGoogle Scholar
  21. Cahill PL, Fidler AE, Hopkins GA, Wood SA (2016) Geographically conserved microbiomes of four temperate water tunicates. Environ Microbiol Rep 8:470­478.  https://doi.org/10.1111/1758-2229.12391 CrossRefPubMedGoogle Scholar
  22. Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643.  https://doi.org/10.1038/ismej.2017.119 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cheng Y, Fox S, Pemberton D, Hogg C, Papenfuss AT, Belov K (2015) The Tasmanian devil microbiome—implications for conservation and management. Microbiome 3:76.  https://doi.org/10.1186/s40168-015-0143-0 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Chiarello M, Villéger S, Bouvier C, Bettarel Y, Bouvier T (2015) High diversity of skin-associated bacterial communities of marine fishes is promoted by their high variability among body parts, individuals and species. FEMS Microbiol Ecol 91(7):fiv061.  https://doi.org/10.1093/femsec/fiv061 CrossRefPubMedGoogle Scholar
  25. Chiarello M, Villéger S, Bouvier C, Auguet JC, Bouvier T (2017) Captive bottlenose dolphins and killer whales harbor a species-specific skin microbiota that varies among individuals. Sci Rep 7:15269.  https://doi.org/10.1038/s41598-017-15220-z CrossRefPubMedPubMedCentralGoogle Scholar
  26. Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270.  https://doi.org/10.1038/nrg3182 CrossRefPubMedPubMedCentralGoogle Scholar
  27. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:14691–14696.  https://doi.org/10.1073/pnas.1005963107 CrossRefPubMedGoogle Scholar
  28. Degli Esposti M, Martinez Romero E (2017) The functional microbiome of arthropods. PLoS ONE 12:e0176573.  https://doi.org/10.1371/journal.pone.0176573 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Degnan PH, Pusey AE, Lonsdorf EV, Goodall J, Wroblewski EE, Wilson ML, Rudicell RS, Hahn BH, Ochman H (2012) Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA 109:13034–13039.  https://doi.org/10.1073/pnas.1110994109 CrossRefPubMedGoogle Scholar
  30. Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, González A, Knight R (2014) Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol 23:1301–1317.  https://doi.org/10.1111/mec.12501 CrossRefPubMedGoogle Scholar
  31. Douglas AE, Werren JH (2016) Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7:e02099–15.  https://doi.org/10.1128/mBio.02099-15 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Eichmiller JJ, Hamilton MJ, Staley C, Sadowsky MJ, Sorensen PW (2016) Environment shapes the fecal microbiome of invasive carp species. Microbiome 4:44.  https://doi.org/10.1186/s40168-016-0190-1 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Erkosar B, Kolly S, van der Meer JR, Kawecki TJ (2017) Adaptation to chronic nutritional stress leads to reduced dependence on microbiota in Drosophila melanogaster. mBio 8:e01496-17.  https://doi.org/10.1128/mBio.01496-17 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Flechas SV, Blasco-Zúñiga A, Merino-Viteri A, Ramírez-Castañeda V, Rivera M, Amézquita A (2017) The effect of captivity on the skin microbial symbionts in three Atelopus species from the lowlands of Colombia and Ecuador. PeerJ 5:e3594.  https://doi.org/10.7717/peerj.3594 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Frey JC, Rothman JM, Pell AN, Nizeyi JB, Cranfield MR, Angert ER (2006) Fecal bacterial diversity in a wild gorilla. Appl Environ Microbiol 72:3788–3792.  https://doi.org/10.1128/AEM.72.5.3788-3792.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fusco G, Minelli A (2010) Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc Lond B 365:547–556.  https://doi.org/10.1098/rstb.2009.0267 CrossRefGoogle Scholar
  37. Gonçalves P, Araújo JR, Di Santo JP (2018) A cross-talk between microbiota-derived short-chain fatty acids and the host mucosal immune system regulates intestinal homeostasis and inflammatory bowel disease. Inflamm Bowel Dis 24:558–572.  https://doi.org/10.1093/ibd/izx029 CrossRefPubMedGoogle Scholar
  38. Hale VL, Tan CL, Niu K, Yang Y, Cui D, Zhao H, Knight R, Amato KR (2016) Effects of field conditions on fecal microbiota. J Microbiol Methods 130:180–188.  https://doi.org/10.1016/j.mimet.2016.09.017 CrossRefPubMedGoogle Scholar
  39. Hernández-Gómez O, Hoverman JT, Williams RN (2017) Cutaneous microbial community variation across populations of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis). Front Microbiol 8:1379.  https://doi.org/10.3389/fmicb.2017.01379 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hu XL, Liu G, Aba S, Wei YT, Zhou JT, Lin SB, Wu H, Zhou M, Hu D, Liu S (2017) Comparative analysis of the gut microbial communities in forest and alpine musk deer using high-throughput sequencing. Front Microbiol 8:572.  https://doi.org/10.3389/fmicb.2017.00572 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jiang H-Y, Ma J-E, Li J, Zhang X-J, Li L-M, He N, Liu H-Y, Luo S-Y, Wu Z-J, Han R-C, Chen J-P (2017) Diets alter the gut microbiome of crocodile lizards. Front Microbiol 8:2073.  https://doi.org/10.3389/fmicb.2017.02073 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Jiménez RR, Sommer S (2017) The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers Conserv 26:763–786.  https://doi.org/10.1007/s10531-016-1272-x CrossRefGoogle Scholar
  43. Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA, Haas AF, Haynes M, Lim YW, McDole T, Nelson CE, Sala E, Sandin SA, Smith JE, Vermeij MJ, Youle M, Rohwer F (2014) Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc Natl Acad Sci USA 111:10227–10232.  https://doi.org/10.1073/pnas.1403319111 CrossRefPubMedGoogle Scholar
  44. Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108:19288–19292.  https://doi.org/10.1073/pnas.1110474108 CrossRefPubMedGoogle Scholar
  45. Kohl KD, Skopec MM, Dearing MD (2014) Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol 2:cou009.  https://doi.org/10.1093/conphys/cou009 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kohl KD, Varner J, Wilkening JL, Dearing MD (2017) Gut microbial communities of American pikas (Ochotona princeps): evidence for phylosymbiosis and adaptations to novel diets. J Anim Ecol 87:323–330.  https://doi.org/10.1111/1365-2656.12692 CrossRefPubMedGoogle Scholar
  47. Kong F, Zhao J, Han S, Zeng B, Yang J, Si X, Yang B, Yang M, Xu H, Li Y (2014) Characterization of the gut microbiota in the red panda (Ailurus fulgens). PLoS ONE 9:e87885.  https://doi.org/10.1371/journal.pone.0087885 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Koskella F, Hall LJ, Metcalf JE (2017) The microbiome beyond the horizon of ecological and evolutionary theory. Nat Ecol Evol 1:1606–1615.  https://doi.org/10.1038/s41559-017-0340-2 CrossRefPubMedGoogle Scholar
  49. Küng D, Bigler L, Davis LR, Gratwicke B, Griffith E, Woodhams DC (2014) Stability of microbiota facilitated by host immune regulation: informing probiotic strategies to manage amphibian disease. PLoS ONE 9:e87101.  https://doi.org/10.1371/journal.pone.0087101 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lemieux-Labonté V, Simard A, Willis CKR, Lapointe FJ (2017) Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5:115.  https://doi.org/10.1186/s40168-017-0334-y CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651.  https://doi.org/10.1126/science.1155725 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Li Y, Guo W, Han S, Kong F, Wang C, Li D, Zhang H, Yang M, Xu H, Zeng B, Zhao J (2015) The evolution of the gut microbiota in the giant and the red pandas. Sci Rep 5:10185.  https://doi.org/10.1038/srep10185 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li X, Yan Q, Ringø E, Wu X, He Y, Yang D (2016) The influence of weight and gender on intestinal bacterial community of wild largemouth bronze gudgeon (Coreius guichenoti, 1874). BMC Microbiol 16:191.  https://doi.org/10.1186/s12866-016-0809-1 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li Y, Hu X, Yang S, Zhou J, Zhang T, Qi L, Sun X, Fan M, Xu S, Cha M, Zhang M, Lin S, Liu S, Hu D (2017a) Comparative analysis of the gut microbiota composition between captive and wild forest musk deer. Front Microbiol 8:1705.  https://doi.org/10.3389/fmicb.2017.01705 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Li H, Qu J, Li T, Yao M, Li J, Li X (2017b) Gut microbiota may predict host divergence time during Glires evolution. FEMS Microbiol Ecol 93:fix009.  https://doi.org/10.1093/femsec/fix009 CrossRefGoogle Scholar
  56. Lizé A, McKay R, Lewis Z (2013) Gut microbiota and kin recognition. Trends Ecol Evol 28:325–326.  https://doi.org/10.1016/j.tree.2012.10.013 CrossRefPubMedGoogle Scholar
  57. Macke E, Callens M, De Meester L, Decaestecker E (2017) Host-genotype dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nat Commun 8:1608.  https://doi.org/10.1038/s41467-017-01714-x CrossRefPubMedPubMedCentralGoogle Scholar
  58. Madison JD, Berg EA, Abarca JG, Whitfield SM, Gorbatenko O, Pinto A, Kerby JL (2017) Characterization of Batrachochytrium dendrobatidis inhibiting bacteria from amphibian populations in Costa Rica. Front Microbiol 8:290.  https://doi.org/10.3389/fmicb.2017.00290 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Manes NP, Shulzhenko N, Nuccio AG, Azeem S, Morgun A, Nita-Lazar A (2017) Multi-omics comparative analysis reveals multiple layers of host signaling pathway regulation by the gut microbiota. mSystems 2:e00107-17.  https://doi.org/10.1128/mSystems.00107-17 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Marchesi JR, Ravel J (2015) The vocabulary of microbiome research: a proposal. Microbiome 3:31.  https://doi.org/10.1186/s40168-015-0094-5 CrossRefPubMedPubMedCentralGoogle Scholar
  61. McCord AI, Chapman CA, Weny G, Tumukunde A, Hyeroba D, Klotz K, Koblings AS, Mbora DN, Cregger M, White BA, Leigh SR, Goldberg TL (2014) Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am J Primatol 76:347–354.  https://doi.org/10.1002/ajp.22238 CrossRefPubMedGoogle Scholar
  62. McFrederick QS, Wcislo WT, Hout MC, Mueller UG (2014) Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol Ecol 88:398–406.  https://doi.org/10.1111/1574-6941.12302 CrossRefPubMedGoogle Scholar
  63. McKenney EA, Maslanka M, Rodrigo A, Yoder AD (2018) Bamboo specialists from two mammalian orders (Primates, Carnivora) share a high number of low-abundance gut microbes. Microb Ecol 76:272.  https://doi.org/10.1007/s00248-017-1114-8 CrossRefPubMedGoogle Scholar
  64. McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, Alexiev A, Amato KR, Metcalf JL, Kowalewski M, Avenant NL, Link A, Di Fiore A, Seguin­Orlando A, Feh C, Orlando L, Mendelson JR, Sanders J, Knight R (2017) The effects of captivity on the mammalian gut microbiome. Integr Comp Biol 57:690–704.  https://doi.org/10.1093/icb/icx090 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Mendes LW, Braga LPP, Navarrete AA, Souza DG, Silva GGZ, Tsai SM (2017) Using metagenomics to connect microbial community biodiversity and functions. Curr Issues Mol Biol 24:103–118.  https://doi.org/10.21775/cimb.024.103 CrossRefPubMedGoogle Scholar
  66. Menke S, Meier M, Mfune JKE, Melzheimer J, Wachter B, Sommer S (2017) Effects of host traits and land-use changes on the gut microbiota of the Namibian black­ backed jackal (Canis mesomelas). FEMS Microbiol Ecol 93:fix123.  https://doi.org/10.1093/femsec/fix123 CrossRefGoogle Scholar
  67. Milan M, Carraro L, Fariselli P, Martino ME, Cavalieri D, Vitali F, Boffo L, Patarnello T, Bargelloni L, Cardazzo B (2018) Microbiota and environmental stress: how pollution affects microbial communities in Manila clams. Aquat Toxicol 194:195–207.  https://doi.org/10.1016/j.aquatox.2017.11.019 CrossRefPubMedGoogle Scholar
  68. Moeller AH, Degnan PH, Pusey AE, Wilson ML, Hahn BH, Ochman H (2012) Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat Commun 3:1179.  https://doi.org/10.1038/ncomms2159 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13:e1002311.  https://doi.org/10.1371/journal.pbio.1002311 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Moran-Ramos S, López-Contreras BE, Canizales-Quinteros S (2017) Gut microbiota in obesity and metabolic abnormalities: a matter of composition or functionality? Arch Med Res 48:735–753.  https://doi.org/10.1016/j.arcmed.2017.11.003 CrossRefPubMedGoogle Scholar
  71. Muegge BD, Kuczynski J, Knights D, Brian D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974.  https://doi.org/10.1126/science.1198719 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Muletz Wolz CR, Yarwood SA, Campbell Grant EH, Fleischer RC, Lips KR (2017) Effects of host species and environment on the skin microbiome of Plethodontid salamanders. J Anim Ecol 87:341–353.  https://doi.org/10.1111/1365-2656.12726 CrossRefPubMedGoogle Scholar
  73. Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F, Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 16:90.  https://doi.org/10.1186/s12866-016-0708-5 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Pascoe EL, Hauffe HC, Marchesi JR, Perkins SE (2017) Network analysis of gut microbiota literature: an overview of the research landscape in non-human animal studies. ISME J 2017:2644–2651.  https://doi.org/10.1038/ismej.2017.133 CrossRefGoogle Scholar
  75. Perry EK, Digby A, Taylor MW (2017) The low-diversity fecal microbiota of the critically endangered kākāpō is robust to anthropogenic dietary and geographic influences. Front Microbiol 8:2033.  https://doi.org/10.3389/fmicb.2017.02033 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Redford KH, Segre JA, Salafsky N, del Rio CM, McAloose D (2012) Conservation and the microbiome. Conserv Biol 26:195–197.  https://doi.org/10.1111/j.1523-1739.2012.01829.x CrossRefPubMedPubMedCentralGoogle Scholar
  77. Roder C, Bayer T, Aranda M, Kruse M, Voolstra CR (2015) Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol Ecol 13:3501–3511.  https://doi.org/10.1111/mec.13251 CrossRefGoogle Scholar
  78. Rodrigo A, Rogers M, Bohlig B (2017) The evolutionary value of helpful microbes: a response to Shapira. Trends Ecol Evol 32:84–85.  https://doi.org/10.1016/j.tree.2016.11.002 CrossRefPubMedGoogle Scholar
  79. Roggenbuck M, Schnell IB, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, Sørensen SJ, Gilbert MT, Graves GR, Hansen LH (2014) The microbiome of New World vultures. Nat Commun 5:5498.  https://doi.org/10.1038/ncomms6498 CrossRefPubMedGoogle Scholar
  80. Sanders JG, Powell S, Kronauer DJC, Vasconcelos HL, Frederickson ME, Pirece NE (2014) Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 23:1268–1283.  https://doi.org/10.1111/mec.12611 CrossRefPubMedGoogle Scholar
  81. Sarmiento-Ramírez JM, van der Voort M, Raaijmakers JM, Diéguez-Uribeondo J (2014) Unravelling the microbiome of eggs of the endangered sea turtle Eretmochelys imbricata identifies bacteria with activity against the emerging pathogen Fusarium falciforme. PLoS ONE 9:e95206.  https://doi.org/10.1371/journal.pone.0095206 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Shapira M (2016) Gut microbiotas and host evolution: scaling up symbiosis. Trends Ecol Evol 31:539–549.  https://doi.org/10.1016/j.tree.2016.03.006 CrossRefGoogle Scholar
  83. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107:20051–20056.  https://doi.org/10.1073/pnas.1009906107 CrossRefPubMedGoogle Scholar
  84. Sharpton TJ (2018) Role of the gut microbiome in vertebrate evolution. mSystems 3:e00174-17.  https://doi.org/10.1128/mSystems.00174-17 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Sommer F, Ståhlman M, Ilkayeva O, Arnemo JM, Kindberg J, Josefsson J, Newgard CB, Fröbert O, Bäckhed F (2016) The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep 14:1655–1661.  https://doi.org/10.1016/j.celrep.2016.01.026 CrossRefPubMedGoogle Scholar
  86. Song SJ, Amir A, Metcalf JL, Amato KR, Xu ZZ, Humphrey G, Knight R (2016) Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems 1:e00021-16.  https://doi.org/10.1128/mSystems.00021-16 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Soverini M, Quercia S, Biancani B, Furlati S, Turroni S, Biagi E, Consolandi C, Peano C, Severgnini M, Rampelli S, Brigidi P, Candela M (2016) The bottlenose dolphin (Tursiops truncatus) faecal microbiota. FEMS Microbio Ecol 92:fiw055.  https://doi.org/10.1093/femsec/fiw055 CrossRefGoogle Scholar
  88. Springer A, Fichtel C, Al-Ghalith GA, Koch F, Amato KR, Clayton JB, Knights D, Kappeler PM (2017) Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux’s sifakas (Propithecus verreauxi). Ecol Evol 7:5732–5745.  https://doi.org/10.1002/ece3.3148 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Stumpf RM, Gomez A, Amato KR, Yeoman CJ, Polk JD, Wilson BA, Nelson KE, White BA, Leigh SR (2016) Microbiomes, metagenomics, and primate conservation: new strategies, tools, and applications. Biol Conserv 199:56–66.  https://doi.org/10.1016/j.biocon.2016.03.035 CrossRefGoogle Scholar
  90. Ushida K, Segawa T, Tsuchida S, Murata K (2016) Cecal bacterial communities in wild Japanese rock ptarmigans and captive Svalbard rock ptarmigans. J Vet Med Sci 78:251–257.  https://doi.org/10.1292/jvms.15-0313 CrossRefPubMedGoogle Scholar
  91. van Dongen WF, White J, Brandl HB, Moodley Y, Merkling T, Leclaire S, Blanchard P, Danchin E, Hatch SA, Wagner RH (2013) Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol 13:11.  https://doi.org/10.1186/1472-6785-13-11 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Vences M, Lyra ML, Kueneman JG, Bletz MC, Archer HM, Canitz J, Handreck S, Randrianiaina RD, Struck U, Bhuju S, Jarek M, Geffers R, McKenzie VJ, Tebbe CC, Haddad CF, Glos J (2016) Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas. Sci Nat 103:25.  https://doi.org/10.1007/s00114-016-1348-1 CrossRefGoogle Scholar
  93. Vogel H, Shukla SP, Engl T, Weiss B, Fischer R, Steiger S, Heckel DG, Kaltenpoth M, Vilcinskas A (2017) The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota. Nat Commun 8:15186.  https://doi.org/10.1038/ncomms15186 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Waite DW, Taylor MW (2015) Exploring the avian gut microbiota: current trends and future directions. Front Microbiol 6:673.  https://doi.org/10.3389/fmicb.2015.00673 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Waite DW, Deines P, Taylor MW (2012) Gut microbiome of the critically endangered New Zealand parrot, the kākāpō (Strigops habroptilus). PLoS ONE 7:e35803.  https://doi.org/10.1371/journal.pone.0035803 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Wan X, Ruan R, McLaughlin RW, Hao Y, Zheng J, Wang D (2016) Fecal bacterial composition of the endangered Yangtze finless porpoises living under captive and semi­natural conditions. Curr Microbiol 72:306–314.  https://doi.org/10.1007/s00284-015-0954-z CrossRefPubMedGoogle Scholar
  97. Wang W, Zheng S, Sharshov K, Cao J, Sun H, Yang F, Wang X, Li L (2016) Distinctive gut microbial community structure in both the wild and farmed Swan goose (Anser cygnoides). J Basic Microbiol 56:1299–1307.  https://doi.org/10.1002/jobm.201600155 CrossRefPubMedGoogle Scholar
  98. Wasimuddin W, Menke S, Melzheimer J, Thalwitzer S, Heinrich S, Wachter B, Sommer S (2017) Gut microbiomes of free-ranging and captive Namibian cheetahs: diversity, putative functions, and occurrence of potential pathogens. Mol Ecol 26:5515–5527.  https://doi.org/10.1111/mec.14278 CrossRefPubMedGoogle Scholar
  99. West AG, Waite DW, Deines P, Bourne DG, Digby A, McKenzie VJ, Taylor MW (2019) The microbiome in threatened species conservation. Biol Conserv 229:85–98.  https://doi.org/10.1016/j.biocon.2018.11.016 CrossRefGoogle Scholar
  100. Williams CL, Dill-McFarland KA, Vandewege MW, Sparks DL, Willard ST, Kouba AJ, Suen G, Brown AE (2016) Dietary shifts may trigger dysbiosis and mucous stools in giant pandas (Ailuropoda melanoleuca). Front Microbiol 7:661.  https://doi.org/10.3389/fmicb.2016.00661 CrossRefPubMedPubMedCentralGoogle Scholar
  101. Woodhams DC, LaBumbard BC, Barnhart KL, Becker MH, Bletz MC, Escobar LA, Flechas SV, Forman ME, Iannetta AA, Joyce MD, Rabemananjara F, Gratwicke B, Vences M, Minbiole KPC (2017) Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microb Ecol 74:1001.  https://doi.org/10.1007/s00248-017-0985-z CrossRefGoogle Scholar
  102. Wu Q, Wang X, Ding Y, Hu Y, Nie Y, Wei W, Ma S, Yan L, Zhu L, Wei F (2017) Seasonal variation in nutrient utilization shapes gut microbiome structure and function in wild giant pandas. Proc Biol Sci 284:20170955.  https://doi.org/10.1098/rspb.2017.0955 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Xie Y, Xia P, Wang H, Yu H, Giesy JP, Zhang Y, Mora MA, Zhang X (2016) Effects of captivity and artificial breeding on microbiota in feces of the red-crowned crane (Grus japonensis). Sci Rep 6:33350.  https://doi.org/10.1038/srep33350 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Xue Z, Zhang W, Wang L, Hou R, Zhang M, Fei L, Zhang X, Huang H, Bridgewater LC, Jiang Y, Jiang C, Zhao L, Pang X, Zhang Z (2015) The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. mBio 6:e00022-15.  https://doi.org/10.1128/mBio.00022-15 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Zhai P, Yang L, Guo X, Wang Z, Guo J, Wang X, Zhu H (2017) MetaComp: comprehensive analysis software for comparative meta-omics including comparative metagenomics. BMC Bioinformatics 18:434.  https://doi.org/10.1186/s12859-017-1849-8 CrossRefPubMedPubMedCentralGoogle Scholar
  106. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735.  https://doi.org/10.1111/j.1574-6976.2008.00123.x CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biodiversity and Molecular Ecology, Research and Innovation CentreFondazione E. MachSan Michele all’AdigeItaly
  2. 2.Department of AnthropologyUniversity of Illinois and Carl R. Woese Institute for Genomic Biology at Urbana-ChampaignUrbanaUSA

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