Symbiont-mediated degradation of dietary carbon sources in social herbivorous insects

Wertz, John T.; Béchade, Benoît

doi:10.1016/bs.aiip.2020.04.001

Cited by 16 publications

(22 citation statements)

References 243 publications

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“…5C; 6). This flexibility is likely pivotal for the ability to track environmental changes and optimize nutrient intake or toxin degradation that maximize host fitness (3,14,15). This is in line with ample evidence for animals filtering their microbial community through exposure to different environments (31,64), including via social interaction in insects (65,66) and primates (23,67,68) or more intricate mechanisms such as coprophagy in wood-feeding cockroaches (24) and trophallaxis in social insects (24,(69)(70)(71)(72).…”

Section: Discussionmentioning

confidence: 75%

“…Intricate associations between animal hosts and their gut microbiota are vital for the evolution and persistence of many animal hosts (1,2). These microbial symbionts facilitate a multitude of functions associated with host nutrient management, immunity and development (1,3), and ultimately impact host adaptation and diversification across environments and dietary niches (e.g., [4][5][6][7][8]. When hosts traits select for specific microbial functions, these can be considered the extended phenotype of the host (9)(10)(11)(12).…”

Section: Introductionmentioning

confidence: 99%

“…When hosts traits select for specific microbial functions, these can be considered the extended phenotype of the host (9)(10)(11)(12). Selection should optimally involve getting a microbiota that is both flexible (i.e., containing environment-specific strains that are likely to enable degradation of environment-specific nutrients and toxins) and consistent (i.e., similar under a defined set of circumstances) rather than subject to random fluctuations (3,(13)(14)(15).…”

Section: Introductionmentioning

confidence: 99%

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Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

Germer

Renelies‐Hamilton

Sillam‐Dussès

et al. 2020

Preprint

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AbstractA multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach vs. termite gut provisioned), and varying diets (matched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rDNA amplicon sequencing. We show that the presence of a pre-existing bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a stronghold and which stabilize the microbiome. However, the subsequent inoculation sources more strongly affect ultimate community composition, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets that consequently strongly impact community functions predicted using PICRUSt2. In conclusion, our findings suggest that inoculations drive communities towards different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments.Contribution to the fieldWhen host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers through interactions with potential colonizers that may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale, but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

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Section: Discussionmentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

Germer

Renelies‐Hamilton

Sillam‐Dussès

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Intricate associations between animal hosts and their gut microbiota are vital for the evolution and persistence of animal hosts ( 1 , 2 ). These microbial symbionts facilitate a multitude of functions associated with host nutrient management, immunity, and development ( 1 , 3 ) and ultimately impact host adaptation and diversification across environments and dietary niches ( 4 – 8 ). When host traits select for specific microbial functions, these can be considered the extended phenotype of the host ( 9 – 12 ).…”

Section: Introductionmentioning

confidence: 99%

“…When host traits select for specific microbial functions, these can be considered the extended phenotype of the host ( 9 – 12 ). Thus, selection should optimally lead to a microbiota that is both functionally flexible (i.e., able to incorporate environment-specific strains that are likely to enable degradation of environment-specific nutrients and toxins) and functionally consistent (i.e., similar under a defined set of circumstances, leading to a reproducible microbiome assembly) rather than be subject to random fluctuations ( 3 , 13 – 15 ). Along those lines, the Anna Karenina principle states that healthy microbiomes are more similar to each other than microbiomes under a range of perturbations ( 16 , 17 ), a paradigm we will use to understand microbiome assembly reproducibility.…”

Section: Introductionmentioning

confidence: 99%

Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly

Renelies‐Hamilton

Germer

Sillam‐Dussès

et al. 2021

mSphere

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A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience, and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach versus termite gut provisioned), and varying diets (matched or unmatched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rRNA gene (rDNA) amplicon sequencing. We show that the presence of a preexisting bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a strong hold and which stabilize the microbiome. However, subsequent inoculation sources more strongly affect ultimate community composition and their ecological networks, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets in ways that consequently impact predicted community functions. In conclusion, our findings suggest that inoculations drive communities toward different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments. IMPORTANCE When host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers, through interactions with potential colonizers, which may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

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Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

D’Amelio

Béchade

et al. 2023

Ecological Monographs

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Sustaining beneficial gut symbioses presents a major challenge for animals, including holometabolous insects. Social insects may meet such challenges through partner fidelity, aided by behavioral symbiont transfer and transgenerational inheritance through colony founders. We address such potential through colony‐wide explorations across 13 eusocial, holometabolous insect species in the ant genus Cephalotes. Through amplicon sequencing, we show that previously characterized worker microbiomes are conserved in soldier castes, that adult microbiomes exhibit trends of phylosymbiosis, and that Cephalotes cospeciate with their most abundant adult‐enriched symbiont. We find, also, that winged queens harbor worker‐like microbiomes prior to colony founding, suggesting vertical inheritance as a means of partner fidelity. Whereas some adult‐abundant symbionts colonize larvae, larval gut microbiomes are uniquely characterized by environmental bacteria from the Enterobacteriales, Lactobacillales, and Actinobacteria. Distributions across Cephalotes larvae suggest more than 40 million years of conserved environmental filtering and, thus, a second sustaining mechanism behind an ancient, developmentally partitioned symbiosis.

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Symbiont-mediated degradation of dietary carbon sources in social herbivorous insects

Cited by 16 publications

References 243 publications

Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

Disentangling the relative roles of vertical transmission, subsequent colonizations and diet on cockroach microbiome assembly

Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly

Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

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