Dataset Information

Models of microbiome evolution incorporating host and microbial selection.

ABSTRACT:

Background

Numerous empirical studies suggest that hosts and microbes exert reciprocal selective effects on their ecological partners. Nonetheless, we still lack an explicit framework to model the dynamics of both hosts and microbes under selection. In a previous study, we developed an agent-based forward-time computational framework to simulate the neutral evolution of host-associated microbial communities in a constant-sized, unstructured population of hosts. These neutral models allowed offspring to sample microbes randomly from parents and/or from the environment. Additionally, the environmental pool of available microbes was constituted by fixed and persistent microbial OTUs and by contributions from host individuals in the preceding generation.

Methods

In this paper, we extend our neutral models to allow selection to operate on both hosts and microbes. We do this by constructing a phenome for each microbial OTU consisting of a sample of traits that influence host and microbial fitnesses independently. Microbial traits can influence the fitness of hosts ("host selection") and the fitness of microbes ("trait-mediated microbial selection"). Additionally, the fitness effects of traits on microbes can be modified by their hosts ("host-mediated microbial selection"). We simulate the effects of these three types of selection, individually or in combination, on microbiome diversities and the fitnesses of hosts and microbes over several thousand generations of hosts.

Results

We show that microbiome diversity is strongly influenced by selection acting on microbes. Selection acting on hosts only influences microbiome diversity when there is near-complete direct or indirect parental contribution to the microbiomes of offspring. Unsurprisingly, microbial fitness increases under microbial selection. Interestingly, when host selection operates, host fitness only increases under two conditions: (1) when there is a strong parental contribution to microbial communities or (2) in the absence of a strong parental contribution, when host-mediated selection acts on microbes concomitantly.

Conclusions

We present a computational framework that integrates different selective processes acting on the evolution of microbiomes. Our framework demonstrates that selection acting on microbes can have a strong effect on microbial diversities and fitnesses, whereas selection on hosts can have weaker outcomes.

SUBMITTER: Zeng Q

PROVIDER: S-EPMC5613328 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Publications

Models of microbiome evolution incorporating host and microbial selection.

Zeng Qinglong Q Wu Steven S Sukumaran Jeet J Rodrigo Allen A

Microbiome 20170925 1

<h4>Background</h4>Numerous empirical studies suggest that hosts and microbes exert reciprocal selective effects on their ecological partners. Nonetheless, we still lack an explicit framework to model the dynamics of both hosts and microbes under selection. In a previous study, we developed an agent-based forward-time computational framework to simulate the neutral evolution of host-associated microbial communities in a constant-sized, unstructured population of hosts. These neutral models allow ...[more]

PMID: 28946894

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Project description:Insects share an intimate relationship with their gut microflora and this symbiotic association has developed into an essential evolutionary outcome intended for their survival through extreme environmental conditions. While it has been clearly established that insects, with very few exceptions, associate with several microbes during their life cycle, information regarding several aspects of these associations is yet to be fully unraveled. Acquisition of bacteria by insects marks the onset of microbial symbiosis, which is followed by the adaptation of these bacterial species to the gut environment for prolonged sustenance and successful transmission across generations. Although several insect-microbiome associations have been reported and each with their distinctive features, diversifications and specializations, it is still unclear as to what led to these diversifications. Recent studies have indicated the involvement of various evolutionary processes operating within an insect body that govern the transition of a free-living microbe to an obligate or facultative symbiont and eventually leading to the establishment and diversification of these symbiotic relationships. Data from various studies, summarized in this review, indicate that the symbiotic partners, i.e., the bacteria and the insect undergo several genetic, biochemical and physiological changes that have profound influence on their life cycle and biology. An interesting outcome of the insect-microbe interaction is the compliance of the microbial partner to its eventual genome reduction. Endosymbionts possess a smaller genome as compared to their free-living forms, and thus raising the question what is leading to reductive evolution in the microbial partner. This review attempts to highlight the fate of microbes within an insect body and its implications for both the bacteria and its insect host. While discussion on each specific association would be too voluminous and outside the scope of this review, we present an overview of some recent studies that contribute to a better understanding of the evolutionary trajectory and dynamics of the insect-microbe association and speculate that, in the future, a better understanding of the nature of this interaction could pave the path to a sustainable and environmentally safe way for controlling economically important pests of crop plants.

Dataset Information

Models of microbiome evolution incorporating host and microbial selection.

Background

Methods

Results

Conclusions

Publications

Models of microbiome evolution incorporating host and microbial selection.

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