Terrestriality and bacterial transfer: A comparative study of gut microbiomes in sympatric Malagasy mammals

Perofsky, Amanda C.; Lewis, Rebecca J.; Meyers, Lauren Ancel

doi:10.1101/293282

Cited by 15 publications

(25 citation statements)

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“…We specifically showed that both constraints shape GMB membership but the phylogenetic scale of analyses can influence the results and their interpretation. Our findings are consistent with recent reports across mammals (Groussin et al, ; Ley et al, ; Nishida & Ochman, ; Perofsky et al, ) and primates (Amato et al, ), including lemurs (Greene et al, in review), that, at gross scales and when feeding strategies are convergent, phylogeny is a strong predictor of GMB structure. Nevertheless, when examining dynamics within lineages of folivores or herbivores compared with frugivores or omnivores, feeding strategy more strongly underlies host–microbiome coadaptation.…”

Section: Study 3 Beyond the Gut: Scent‐gland Microbiomes Vary By Bodsupporting

confidence: 93%

“…Researchers have documented within‐species variation in GMB structure relative to seasonal food availability (Springer et al, ), habitat quality (Bennett et al, ), and social dynamics (Perofsky, Lewis, Abondano, Di Fiore, & Meyers, ; Raulo et al, ). Increasingly, researchers have adopted small‐scale comparative approaches, investigating GMB composition across host populations, species, and habitat types (Greene et al, in review; Perofsky, Lewis, & Meyers, ; Umanets et al, ). Opportunities for longitudinal sampling and experimental manipulation using captive populations have facilitated studies on the timing of microbiome acquisition across host ontogenetic development (McKenney, Rodrigo, & Yoder, ), patterns of recovery from enteric infection (McKenney, Greene, Drea, & Yoder, ), and response to changing dietary quality (Greene, McKenney, O'Connell, & Drea, ).…”

Section: Introductionmentioning

confidence: 99%

“…One topic of discussion involves the respective roles of host phylogenetic relationships and feeding ecology (Delsuc et al, ; Groussin et al, ; Ley et al, ; Nishida & Ochman, ). On the one hand, the role of phylogenetic placement dominates when analyses are scaled broadly across mammalian taxa (Amato et al, ; Groussin et al, ; Ley et al, ; Nishida & Ochman, ; Perofsky et al, ) or within lineages that are characterized by limited species diversity (Ochman et al, ). On the other hand, shared feeding strategies can lead to GMB convergence across distant relatives (Delsuc et al, ).…”

Section: Introductionmentioning

confidence: 99%

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The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

Greene

Bornbusch

McKenney

et al. 2019

American J Primatol

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Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host-microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure.Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage-specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research.We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent-gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host-microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis-driven research. RESEARCH HIGHLIGHTS• Comparing gut microbiomes in diverse lemurs shows that community structure reflects host phylogeny at broad scales, but when controlling for evolutionary time, feeding strategy underlies the strength of host-microbe coadaptation at narrow scales.Am J Primatol. 2019;81:e22974.wileyonlinelibrary.com/journal/ajp

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Section: Study 3 Beyond the Gut: Scent‐gland Microbiomes Vary By Bodsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

Greene

Bornbusch

McKenney

et al. 2019

American J Primatol

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“…) or even at a similar level in the forest canopy (Perofsky et al . ) converge in their microbiota, community composition remains most strongly predicted by species identity. By contrast, studies on the gut microbiota of distantly related artiodactyl species (Moeller et al .…”

Section: Discussionmentioning

confidence: 99%

Species identity dominates over environment in shaping the microbiota of small mammals

2019

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The mammalian gut microbiota is considered pivotal to host fitness, yet the determinants of community composition remain poorly understood. Laboratory studies show that environmental factors, particularly diet, are important, while comparative work emphasises host genetics. Here, we compare the influence of host genetics and the environment on the microbiota of sympatric small mammal species (mice, voles, shrews) across multiple habitats. While sharing a habitat caused some microbiota convergence, the influence of species identity dominated. In all three host genera examined, an individual's microbiota was more similar to conspecifics living elsewhere than to heterospecifics at the same site. Our results suggest this species‐specificity arises in part through host‐microbe codiversification. Stomach contents analysis suggested that diet also shapes the microbiota, but where diet is itself influenced by species identity. In this way, we can reconcile the importance of both diet and genetics, while showing that species identity is the strongest predictor of microbiota composition.

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“…An insu cient supply with these materials causes an impairment of ruminal development and, in consequence, a reduced (microbial) digestive capacity [3]. Another important factor is the GIT microbiome itself, which is believed to be shaped by animal genetics, diet, environmental (geographic) parameters [4], and social contact patterns [5,6,7].…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic and functional adaption of the gastrointestinal microbiome of goats kept at high altitude (4800 m) under intensive or extensive rearing conditions

Zhang

et al. 2020

Preprint

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Background: The gut microbiota composition is influenced by the diet as well as the environment in both wild and domestic animals. Although the rumen microbiome in herbivorous ruminants has been studied intensively, there is a lack of data regarding the simultaneous adaption of the rumen and hindgut metagenome as affected by different feeding systems in extreme environments. Therefore, we studied the effects of two feeding systems, grazing and drylot, on the rumen and hindgut microbiome composition of semi-feral Tibetan goats kept at high altitude (~4800 m). 16S rRNA gene sequencing and metagenomic analysis were conducted on DNA extracts from the contents and mucosal layer of different sections of the gastrointestinal tract (rumen, cecum, and colon).Results: Intensive drylot feeding resulted in significantly higher zootechnical performance, narrower ruminal acetate: propionate ratios and a drop in the average rumen pH at slaughter to ~5.04. In response, the ruminal microbiome of drylot goats expressed a significantly lower diversity compared to the grazing animals. Otherwise, hindgut microbial adaption appeared to more diverse in the drylot group suggesting a higher influx of undegraded complex non-starch polysaccharides from the rumen. Despite their higher fiber levels in the diet, grazing goats exhibited lower counts of Methanobrevibacter and genes associated with the hydrogenotrophic methanogenesis pathway, presumably reflecting the scarce dietary conditions (low energy density) when rearing goats on pasture from extreme alpine environments. These conditions appeared to promote a relevant abundance of bacitracin genes, which potentially benefits the host's adaption to harsh environmental conditions. In parallel, we recognized a significant increase in the abundance of antibiotic resistance genes in the digestive tracts of drylot animals.Conclusion: In summary, this study provides a deeper insight in the phylogenetic and functional adaption of the gastrointestinal microbiome of goats subject to intensive drylot and extensive pasture rearing conditions at high altitude.

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Terrestriality and bacterial transfer: A comparative study of gut microbiomes in sympatric Malagasy mammals

Abstract: 17The gut microbiomes of mammals appear to mirror their hosts ' phylogeny, 18 suggesting a shared history of co-speciation. Yet

Cited by 15 publications

References 95 publications

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

Species identity dominates over environment in shaping the microbiota of small mammals

Phylogenetic and functional adaption of the gastrointestinal microbiome of goats kept at high altitude (4800 m) under intensive or extensive rearing conditions

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