Experimental Evidence for Adaptation to Species-Specific Gut Microbiota in House Mice

Moeller, Andrew H.; Gomes-Neto, João Carlos; Mantz, Sara; Kittana, Hatem; Muñoz, Rafael R. Segura; Schmaltz, Robert; Ramer‐Tait, Amanda E.; Nachman, Michael W.

doi:10.1128/msphere.00387-19

Cited by 37 publications

(37 citation statements)

References 43 publications

(39 reference statements)

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“…This was particularly evident for some bacterial taxa such as Actinobacteria (sp.1 and sp.2), Geobacillus and Wolbachia, which were hosted by P. horvathi and P. tridentatus ( Figure 5). The results are consistent with recent studies showing strong associations between host phylogenetic divergence and phylogenetic divergence of the associated microbiome in several taxa, including humans [72,73], mice [74], birds [75], lizards [76] and insects [77].…”

Section: Codiversification Between Water Striders and Their Microbiomesupporting

confidence: 92%

The Microbiome of Neotropical Water Striders and Its Potential Role in Codiversification

Castillo

Saltonstall

Arias

et al. 2020

Insects

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Insects host a highly diverse microbiome, which plays a crucial role in insect life. However, the composition and diversity of microbiomes associated with Neotropical freshwater insects is virtually unknown. In addition, the extent to which diversification of this microbiome is associated with host phylogenetic divergence remains to be determined. Here, we present the first comprehensive analysis of bacterial communities associated with six closely related species of Neotropical water striders in Panama. We used comparative phylogenetic analyses to assess associations between dominant bacterial linages and phylogenetic divergence among species of water striders. We found a total of 806 16S rRNA amplicon sequence variants (ASVs), with dominant bacterial taxa belonging to the phyla Proteobacteria (76.87%) and Tenericutes (19.51%). Members of the α- (e.g., Wolbachia) and γ- (e.g., Acinetobacter, Serratia) Proteobacteria, and Mollicutes (e.g., Spiroplasma) were predominantly shared across species, suggesting the presence of a core microbiome in water striders. However, some bacterial lineages (e.g., Fructobacillus, Fluviicola and Chryseobacterium) were uniquely associated with different water strider species, likely representing a distinctive feature of each species’ microbiome. These findings indicate that both host identity and environmental context are important drivers of microbiome diversity in water striders. In addition, they suggest that diversification of the microbiome is associated with diversification in water striders. Although more research is needed to establish the evolutionary consequences of host-microbiome interaction in water striders, our findings support recent work highlighting the role of bacterial community host-microbiome codiversification.

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Section: Codiversification Between Water Striders and Their Microbiomesupporting

confidence: 92%

The Microbiome of Neotropical Water Striders and Its Potential Role in Codiversification

Castillo

Saltonstall

Arias

et al. 2020

Insects

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“…Similarly, germ-free mice exhibit a range of changes in growth rate and fecundityrelated phenotypes (Dubos and Schaedler, 1960). In addition, the host-species specific microbiota appears to be a key regulator of growth phenotypes, as house mice (Mus musculus domesticus) inoculated with the gut microbiota of closely related host species display altered growth curves than when inoculated with their own gut microbiota (Moeller et al, 2019). These results suggest that disruption of the gut microbiota by thermal stress could ultimately affect host growth and reproductive traits, but this hypothesis has not been tested with experiment.…”

Section: Host Life History Traitsmentioning

confidence: 99%

“…In addition, gut-microbiota transplant experiments into axenic hosts have revealed that variation in the microbiota can generate variation in host phenotypes (Faith et al, 2014;Gould et al, 2018). Recently, this gut-microbiota driven variation in host phenotype has been implicated in the adaptive evolution of host populations (Rudman et al, 2019) and species (Moeller et al, 2019), further suggested that the presence of specific microorganisms in the gut is important for host fitness. As temperature regimes change globally, any effect that these changes have on the composition of animal gut microbial communities may alter their functions and lead to consequences for host phenotypes and fitness.…”

Section: Introductionmentioning

confidence: 99%

The Effects of Temperature on Animal Gut Microbiomes

2020

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Temperature is a prominent abiotic environmental variable that drives the adaptive trajectories of animal lineages and structures the composition of animal communities. Global temperature regimes are expected to undergo rapid shifts in the next century, yet for many animal taxa we lack an understanding of the consequences of these predicted shifts for animal populations. In this review, we synthesize recent evidence that temperature variation shapes the composition and function of animal gut microbiomes, key regulators of host physiology, with potential consequences for host population responses to climate change. Several recent studies spanning a range of animal taxa, including Chordata, Arthropoda, and Mollusca, have reported repeatable associations between temperature and the community composition and function of the gut microbiome. In several cases, the same microbiome responses to temperature have been observed across distantly related animal taxa, suggesting the existence of conserved mechanisms underlying temperature-induced microbiome plasticity. Extreme temperatures can disrupt the stability of alpha-diversity within the gut microbiomes individual hosts and generate beta-diversity among microbiomes within host populations. Microbiome states resulting from extreme temperatures have been associated, and in some cases causally linked, with both beneficial and deleterious effects on host phenotypes. We propose routes by which temperature-induced changes in the gut microbiome may impact host fitness, including effects on colonization resistance in the gut, on host energy and nutrient assimilation, and on host life history traits. Cumulatively, available data indicate that disruption of the gut microbiome may be a mechanism by which changing temperatures will impact animal fitness in wild-living populations.

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“…It has been shown that the composition of the gut microbiota can have profound effects on the host’s physiology and morphology, as well as behaviour [ 3 – 8 ]. Moreover, between-species divergence in the gut microbiota composition could play a role in the establishment of reproductive isolation between species and thus in generating species diversity [ 6 , 9 , 10 ]. Despite recent intensive research on variation in the gut microbiota composition within and between vertebrate species [ 1 , 11 – 14 ] the factors that generate the gut microbial diversity are still not sufficiently understood, especially in non-mammalian taxa.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota in two recently diverged passerine species: evaluating the effects of species identity, habitat use and geographic distance

et al. 2021

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Background It has been proposed that divergence in the gut microbiota composition between incipient species could contribute to their reproductive isolation. Nevertheless, empirical evidence for the role of gut microbiota in speciation is scarce. Moreover, it is still largely unknown to what extent closely related species in the early stages of speciation differ in their gut microbiota composition, especially in non-mammalian taxa, and which factors drive the divergence. Here we analysed the gut microbiota in two closely related passerine species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (Luscinia luscinia). The ranges of these two species overlap in a secondary contact zone, where both species occasionally hybridize and where interspecific competition has resulted in habitat use differentiation. Results We analysed the gut microbiota from the proximal, middle and distal part of the small intestine in both sympatric and allopatric populations of the two nightingale species using sequencing of bacterial 16S rRNA. We found small but significant differences in the microbiota composition among the three gut sections. However, the gut microbiota composition in the two nightingale species did not differ significantly between either sympatric or allopatric populations. Most of the observed variation in the gut microbiota composition was explained by inter-individual differences. Conclusions To our knowledge, this is the first attempt to assess the potential role of the gut microbiota in bird speciation. Our results suggest that neither habitat use, nor geographical distance, nor species identity have strong influence on the nightingale gut microbiota composition. This suggests that changes in the gut microbiota composition are unlikely to contribute to reproductive isolation in these passerine birds.

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Experimental Evidence for Adaptation to Species-Specific Gut Microbiota in House Mice

Cited by 37 publications

References 43 publications

The Microbiome of Neotropical Water Striders and Its Potential Role in Codiversification

The Microbiome of Neotropical Water Striders and Its Potential Role in Codiversification

The Effects of Temperature on Animal Gut Microbiomes

Gut microbiota in two recently diverged passerine species: evaluating the effects of species identity, habitat use and geographic distance

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