1. Microbial symbionts play a crucial role in the development, health, and homeostasis of their hosts. However, the eco‐evolutionary conditions shaping these relationships and the evolutionary scale at which host–microbiome interactions may diverge warrant further investigation, especially in non‐model systems. This study examines the impact of reciprocal gut microbiome transplants between two ecologically very similar, sympatric, and syntopic dung beetle sister species. 2.Onthophagus vaccaandOnthophagus mediuswere specifically used to compare the growth, development, and fitness outcomes of individuals that were either (i) reared in the presence of a microbiome provided by a mother of the same species (“self‐inoculated”), (ii) forced to develop with a microbiome derived from a heterospecific mother (“cross‐inoculated”), or (iii) reared without a maternally transmitted microbiome. 3. This study found that individuals reared in the absence of a maternally derived gut microbiome incur detrimental changes in survival, as well as in several metrics signalling normative development. Furthermore, such negative effects are only partly rescued through inoculation with a heterologous microbiome. 4. Collectively, this study's results suggest that inoculation with a species‐specific, maternally transmitted microbiome is critical for normative development, that the significance of maternally derived microbiota for host survival differs across species, and that the phenotypic outcomes resulting from host–microbiome interactions may diverge even between closely related, ecologically similar host species.
more »
« less
Between‐partner concordance of vertically transmitted gut microbiota diminishes reproductive output in the dung beetle Onthophagus taurus
Abstract In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, usingOnthophagus taurus(Schreber, 1759) and its sister speciesO. illyricus(Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called thepedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (SelfandCrossinoculation treatments, respectively). We then crossed the resulting adultO. taurusin three combinations (Selffemale XSelfmale;Selffemale XCrossmale;Crossfemale XSelfmale). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, theSelfXSelfline would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between‐partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre‐copulatory isolation as evidenced by reduced sperm transfer in theSelfXSelfline. This pattern is consistent either with microbiome‐mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.
more »
« less
- Award ID(s):
- 1901680
- PAR ID:
- 10396426
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Physiological Entomology
- Volume:
- 48
- Issue:
- 1
- ISSN:
- 0307-6962
- Page Range / eLocation ID:
- p. 14-23
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Gut microbiomes provide numerous physiological benefits for host animals. The role of bacterial members of microbiomes in host physiology is well-documented. However, much less is known about the contributions and interactions of fungal members of the microbiome even though fungi are significant components of many microbiomes, including those of humans and insects. Here, we used antibacterial and antifungal drugs to manipulate the gut microbiome of a Hawaiian picture-wingDrosophilaspecies,D. grimshawi, and identified distinct, sex-specific roles for the bacteria and fungi in microbiome community stability and reproduction. Female oogenesis, fecundity and mating drive were significantly diminished when fungal communities were suppressed. By contrast, male fecundity was more strongly affected by bacterial but not fungal populations. For males and females, suppression of both bacteria and fungi severely reduced fecundity and altered fatty acid levels and composition, implicating the importance of interkingdom interactions on reproduction and lipid metabolism. Overall, our results reveal that bacteria and fungi have distinct, sexually-dimorphic effects on host physiology and interkingdom dynamics in the gut help to maintain microbiome community stability and enhance reproduction.more » « less
-
Abstract All animals carry specialized microbiomes, and their gut microbiota are continuously released into the environment through excretion of waste. Here we propose themeta-gutas a novel conceptual framework that addresses the ability of the gut microbiome released from an animal to function outside the host and alter biogeochemical processes mediated by microbes. We demonstrate this dynamic in the hippopotamus (hippo) and the pools they inhabit. We used natural field gradients and experimental approaches to examine fecal and pool water microbial communities and aquatic biogeochemistry across a range of hippo inputs. Sequencing using 16S RNA methods revealed community coalescence between hippo gut microbiomes and the active microbial communities in hippo pools that received high inputs of hippo feces. The shared microbiome between the hippo gut and the waters into which they excrete constitutes ameta-gutsystem that could influence the biogeochemistry of recipient ecosystems and provide a reservoir of gut microbiomes that could influence other hosts. We propose thatmeta-gutdynamics may also occur where other animal species congregate in high densities, particularly in aquatic environments.more » « less
-
Suen, Garret (Ed.)ABSTRACT The gut microbiome is a symbiotic microbial community associated with the host and plays multiple important roles in host physiology, nutrition, and health. A number of factors have been shown to influence the gut microbiome, among which diet is considered to be one of the most important; however, the relationship between diet composition and gut microbiota in wild mammals is still not well recognized. Herein, we characterized the gut microbiota of bats and examined the effects of diet, host taxa, body size, gender, elevation, and latitude on the gut microbiota. The cytochrome C oxidase subunit I (COI) gene and 16S rRNA gene amplicons were sequenced from the feces of eight insectivorous bat species in southern China, includingMiniopterus fuliginosus,Aselliscus stoliczkanus,Myotis laniger,Rhinolophus episcopus,Rhinolophus osgoodi,Rhinolophus ferrumequinum,Rhinolophus affinis,andRhinolophus pusillus. The results showed that the composition of gut microbiome and diet exhibited significant differences among bat species. Diet composition and gut microbiota were significantly correlated at the order, family, genus, and operational taxonomic unit levels, while certain insects had a marked effect on the gut microbiome at specific taxonomic levels. In addition, elevation, latitude, body weight of bats, and host species had significant effects on the gut microbiome, but phylosymbiosis between host phylogeny and gut microbiome was lacking. These findings clarify the relationship between gut microbiome and diet and contribute to improving our understanding of host ecology and the evolution of the gut microbiome in wild mammals. IMPORTANCEThe gut microbiome is critical for the adaptation of wildlife to the dynamic environment. Bats are the second-largest group of mammals with short intestinal tract, yet their gut microbiome is still poorly studied. Herein, we explored the relationships between gut microbiome and food composition, host taxa, body size, gender, elevation, and latitude. We found a significant association between diet composition and gut microbiome in insectivorous bats, with certain insect species having major impacts on gut microbiome. Factors like species taxa, body weight, elevation, and latitude also affected the gut microbiome, but we failed to detect phylosymbiosis between the host phylogeny and the gut microbiome. Overall, our study presents novel insights into how multiple factors shape the bat’s gut microbiome together and provides a study case on host-microbe interactions in wildlife.more » « less
-
Abstract The composition of mammalian gut microbiomes is highly conserved within species, yet the mechanisms by which microbiome composition is transmitted and maintained within lineages of wild animals remain unclear. Mutually compatible hypotheses exist, including that microbiome fidelity results from inherited dietary habits, shared environmental exposure, morphophysiological filtering and/or maternal effects. Interspecific hybrids are a promising system in which to interrogate the determinants of microbiome composition because hybrids can decouple traits and processes that are otherwise co‐inherited in their parent species. We used a population of free‐living hybrid zebras (Equus quagga×grevyi) in Kenya to evaluate the roles of these four mechanisms in regulating microbiome composition. We analysed faecal DNA for both thetrnL‐P6 and the 16S rRNA V4 region to characterize the diets and microbiomes of the hybrid zebra and of their parent species, plains zebra (E. quagga) and Grevy's zebra (E. grevyi). We found that both diet and microbiome composition clustered by species, and that hybrid diets and microbiomes were largely nested within those of the maternal species, plains zebra. Hybrid microbiomes were less variable than those of either parent species where they co‐occurred. Diet and microbiome composition were strongly correlated, although the strength of this correlation varied between species. These patterns are most consistent with the maternal‐effects hypothesis, somewhat consistent with the diet hypothesis, and largely inconsistent with the environmental‐sourcing and morphophysiological‐filtering hypotheses. Maternal transmittance likely operates in conjunction with inherited feeding habits to conserve microbiome composition within species.more » « less
An official website of the United States government
