Application of ecological and evolutionary theory to microbiome community dynamics across systems

Abstract

A fundamental aim of microbiome research is to understand the factors that influence the assembly and stability of host-associated microbiomes, and their impact on host phenotype, ecology and evolution. However, ecological and evolutionary theories applied to predict microbiome community dynamics are largely based on macroorganisms and lack microbiome-centric hypotheses that account for unique features of the microbiome. This special feature sets out to drive advancements in the application of eco-evolutionary theory to microbiome community dynamics through the development of microbiome-specific theoretical and conceptual frameworks across plant, human and non-human animal systems. The feature comprises 11 research and review articles that address: (i) the effects of the microbiome on host phenotype, ecology and evolution; (ii) the application and development of ecological and evolutionary theories to investigate microbiome assembly, diversity and stability across broad taxonomic scales; and (iii) general principles that underlie microbiome diversity and dynamics. This cross-disciplinary synthesis of theoretical, conceptual, methodological and analytical approaches to characterizing host–microbiome ecology and evolution across systems addresses key research gaps in the field of microbiome research and highlights future research priorities.

Improving Taxonomic Delimitation of Fungal Species in the Age of Genomics and Phenomics

“…Distinguishing fungal species boundaries is an important practical concern for researchers seeking to address questions related to biodiversity, species interactions, biogeography, ecological processes, and evolutionary dynamics. Conceptually, eco-evolutionary theory recognizes the interplay between ecological processes and evolutionary dynamics in shaping genetic, phenotypic, and functional traits ( Brunner et al, 2019 ; McDonald et al, 2020 ). Similarly, integrative taxonomy combines technical evidence from many types of observations (e.g., ecological, phylogenetic, morphological, etc.)…”

“…Secondly, we encourage the application of eco-evolutionary theory to conceptualize experimental manipulation of fungal species interactions. Experimental evolution studies are particularly well-suited to explore how fungal communities may shape host health ( Koskella and Bergelson, 2020 ; Morella et al, 2020 ) and contribute to microbe-microbe interactions that drive speciation ( McDonald et al, 2020 ). Additionally, designing and interpreting research outcomes with concepts such as phylosymbiosis ( Kohl, 2020 ; McDonald et al, 2020 ) and the geographic mosaic of co-evolution ( Medeiros et al, 2018 ; Fernandes et al, 2019 ) can improve understanding of drivers of microbial ecology and evolution.…”

“…Eco-evolutionary dynamics recognize the role of ecological properties (e.g., spatial heterogeneity, habitat conditions, dispersal, and assembly patterns) and evolutionary trajectories (e.g., life history traits, co-evolution mosaics, intra- and inter-population selection) in reciprocally influencing one another ( Brunner et al, 2019 ). As such, applying an eco-evolutionary framework to microbial interactions has offered new insight into the processes shaping communities and species interactions ( McDonald et al, 2020 ). For example, the framework has given rise to the coupling of molecular and microbiological tools with theoretical approaches toward genetics, phenotypic evolution, species co-evolution, and ecology ( Saikkonen et al, 2020 ).…”

Microbial Ecology and Evolution Are Essential for Understanding Pandemics

“…In the years leading up to the COVID-19 pandemic, biologists had gradually moved away from thinking of microbes primarily as disease-causing “germs” and began to appreciate the diverse communities of nonpathogenic microbes that often colonize hosts—i.e., the host-associated microbiome ( 4 , 5 ). In microbiome science, as in much work on SARS-CoV-2, the fundamental questions are also often inherently ecological or evolutionary in nature, as we highlight in Table 1 (see also references 6 – 8 ). Answering these questions is necessary and urgent, both for controlling the spread of SARS-CoV-2 and other novel pathogens and for developing new microbial therapies and applications that leverage the potential of beneficial microbiota ( 9 ).…”

Proceedings B 2020: the year in review

“…This year we feature the 'Application of ecological and evolutionary theory to microbiome community dynamics across systems', guest edited by James McDonald (Bangor University), Julian Marchesi (Imperial College, London & Cardiff University) and Britt Koskella (University of California, Berkley). This Special Feature comprises 11 articles plus an introduction [3]. There is now growing appreciation that host-associated microbiomes play a critical role in ecology and evolution, and recent research on the factors governing their assembly, diversity and stability has provided novel perspectives on a range of topics including: horizontal gene transfer, rapid evolution and the production of antimicrobial compounds.…”