The study of host–microbiome (co)evolution across levels of selection

Abstract

Microorganismal diversity can be explained in large part by selection imposed from both the abiotic and biotic environments, including—in the case of host-associated microbiomes—interactions with eukaryotes. As such, the diversity of host-associated microbiomes can be usefully studied across a variety of scales: within a single host over time, among host genotypes within a population, between populations and among host species. A plethora of recent studies across these scales and across diverse systems are: (i) exemplifying the importance of the host genetics in shaping microbiome composition; (ii) uncovering the role of the microbiome in shaping key host phenotypes; and (iii) highlighting the dynamic nature of the microbiome. They have also raised a critical question: do these complex associations fit within our existing understanding of evolution and coevolution, or do these often intimate and seemingly cross-generational interactions follow novel evolutionary rules from those previously identified? Herein, we describe the known importance of (co)evolution in host–microbiome systems, placing the existing data within extant frameworks that have been developed over decades of study, and ask whether there are unique properties of host–microbiome systems that require a paradigm shift. By examining when and how selection can act on the host and its microbiome as a unit (termed, the holobiont), we find that the existing conceptual framework, which focuses on individuals, as well as interactions among individuals and groups, is generally well suited for understanding (co)evolutionary change in these intimate assemblages. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

Metagenomic analysis of the cow, sheep, reindeer and red deer rumen

“…We are aware that the sample sizes for our study are small and unequal numbers of samples were included per group, therefore any conclusions about differences between the microbiota of ruminant species should be drawn cautiously. However, our data are supportive of the hypothesis that there are host species-specific rumen microbiota at the strain and species level, potentially due to the co-evolution of the microbiome and host 37 , but that these differences do not necessarily translate into large differences in the types of CAZymes expressed. While we found that there were significant differences between the abundances of CAZymes and KEGG orthologs between ruminant species, most CAZymes and KEGG orthologs were present in all ruminant species.…”

Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume‐rhizobium mutualism

“…Overall, our study suggests that mutualistic microbes may act like facilitator species during ecological succession, promoting the establishment of their hosts while maintaining separate fitness interests that maintain selection for antagonistic loci. Although holobiont theory has sometimes been used to characterize plant-microbe interactions (Hassani et al 2018), the mismatches we detect between host and symbiont fitness interests suggest that individual populations of hosts and symbionts are more appropriate units of selection in this system (Koskella and Bergelson 2020).…”

The Origin of Niches and Species in the Bacterial World

“…As in the case of the sterile newborns, there is there a “founder effect” involving the neighbor bacterial populations from kin individuals. This core phyla microbiota in mammals can diverge depending on the mammals’ evolution and diversification ( Moeller and Sanders, 2020 ), mostly at the lower taxonomic ranks where particular types of bacteria tend to be associated with mammalian lineages, which implies a host niche-microbiota coevolution, probably based on differences in the intestinal chemosphere, including adaptation to diet and the local immune response ( Shapira, 2016 ; Nishida and Ochman, 2018 ; Koskella and Bergelson, 2020 ). The need for maintaining the basic intestinal microbial niche under differing diets might have influenced the enlargement (possible niche construction) of parts of the gut (as foregut fermenters) to ensure long-term microbe-food interaction ( Ley et al, 2008a , b ).…”