The role of the microbiome in host evolution

Kolodny, Oren; Callahan, Benjamin J.; Douglas, Angela E.

doi:10.1098/rstb.2019.0588

Cited by 39 publications

(33 citation statements)

References 16 publications

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“…The GM may drive the evolution of immune genes Variation in the GM can affect traits important to the host's own tness [127], including host immune function [128], the severity of diseases [129], and ultimately, survival [130], providing the potential for host evolutionary adaptation [131]. If immune genes can regulate tness through modulation of the microbiome, then it is plausible that the microbiome can also in uence selection on immune genes.…”

Section: Mhc Variation Shapes Gm Variationmentioning

confidence: 99%

Immunogenetic Variation Shapes the Gut Microbiome in a Natural Vertebrate Population

Davies

Worsley

Maher

et al. 2021

Preprint

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Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host’s traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host’s GM. However, despite this - and the documented importance of both GM and MHC variation to individual fitness - few studies have investigated the association between the GM and MHC in the wild. Results: We characterised MHC class I (MHC-I), MHC class II (MHC-II), and GM variation in individuals within a natural population of the Seychelles warbler, Acrocephalus sechellensis. We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host intrinsic traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. We found that MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). GM diversity was also positively correlated with genome-wide heterozygosity and varied with host age and field period.Conclusions: These results suggest that components of the host’s immune system play a role in shaping the GM of wild animals. Host genotype – specifically, adaptive immune receptor MHC-I alleles – can modulate the GM, although whether this occurs directly, or indirectly through effects on host health is unclear. To our knowledge this is the first-time individual MHC-I variation has been shown to be associated with differences in GM characteristics in a natural population. Importantly, it suggests that host–microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations.

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Section: Mhc Variation Shapes Gm Variationmentioning

confidence: 99%

Immunogenetic Variation Shapes the Gut Microbiome in a Natural Vertebrate Population

Davies

Worsley

Maher

et al. 2021

Preprint

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“…However, microbes also mediate critical plant functional traits and patterns of fitness, and therefore can facilitate adaptation to other biotic and abiotic selective agents (e.g., drought, herbivory, metal tolerance). Microbial‐mediation of adaptive responses has recently come to the attention of evolutionary ecologists and is changing how the process of adaptation is viewed (Kolodny et al, 2020). It is an interesting, and open question, in what ways and how frequently plant interactions with the environment are facilitated by microbes.…”

Section: Introductionmentioning

confidence: 99%

Microbe‐mediated adaptation in plants

2021

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Plant-associated microbes affect a wide-variety of plant functional traits, and thus they likely affect patterns of plant local adaptation. However, the role of microbes in plant local adaptation is rarely tested. In a survey of the plant local adaptation literature, I found that the vast majority of studies that report local adaptation (94%) performed transplants into microbe-containing soils and measured traits that are microbemediated. In these studies, microbe-mediated effects are confounded with plant genotype effects. For my dissertation research, I sought to describe the phenomenon of microbe-mediated adaptation and provide a definitive test using a modified reciprocal transplant experiments that moved seeds and microbes into two habitats. Here I present my dissertation work in three chapters:In my first chapter, I propose two ways in which microbes facilitate patterns of adaptation for plants, microbe-mediated local adaptation and microbe-mediated adaptive plasticity. Microbe-mediated local adaptation is when plant genotypes have higher fitness at their home site because of a genotype-specific affiliation with locally important microbe(s). Microbe-mediated adaptive plasticity is when a plant genotype has higher fitness in multiple habitats because it demonstrates plasticity in associating with locally important microbes.In my second chapter, I describe soil conditions, plant phenotype, and microbial communities in two habitats. I used high-throughput tagged amplicon sequencing of SSU-rRNA genes (for bacteria) and ITS1 (for fungi) to characterize the root microbiome of Saint John's wort, Hypericum perforatum. At each root sampling location, I quantified soil characteristics to evaluate habitat variables that are correlated with root microbial communities. I also collected information on plant growth and fecundity for each focal plant to identify microbes that are correlated with plant phenotype. We found that bacterial and fungal communities were significantly different between habitats. Community differences were correlated with soil nitrogen and pH, and two taxa in the phylum Actinobacteria were significantly correlated with plant height.In my third chapter, I test for microbe-mediated adaptation using the two habitats, limestone barrens (alvars) and old-fields, described in chapter two. I conducted reciprocal transplant experiments in two years, exploring microbe effects on plant germination, survival, and growth. I found that alvar seeds had higher probability of germination when transplanted into home soils with microbes, but only when transplanted into their home habitat. Similarly, alvar seedlings had a higher probability of survival when transplanted into their home live soils, but here transplant site was unimportant. I also found local microbes inhibited local adaptation for old-field seedlings and facilitated local adaptation for alvar seedlings. My results indicate that microbial mutualists were important for plants growing in marginal alvar habitats, and that microbes changed patterns of local...

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“…One of the mechanisms influencing behavioral traits could be changes in animal’s microbiome, caused by a specific niche formed by cohabitation with humans. Gut microbiome was recently called a “forgotten organ” (O’Hara and Shanahan, 2006) and became a focus of new theory – microbial involvement in evolutionary processes (Kolodny et al, 2020). All species have species-specific gut microbiome, influencing their adaptation and diversification, helping with challenges of food availability, phenotypic plasticity, innate, and adaptive immunity.…”

Section: Microbiome and Behavioral Traitsmentioning

confidence: 99%

“…All species have species-specific gut microbiome, influencing their adaptation and diversification, helping with challenges of food availability, phenotypic plasticity, innate, and adaptive immunity. Generally, gut microbiome is an important environmental factor and selective force, forming adaptive evolution of animal’s diet, phenotypic plasticity, gut morphology, and immunity (Kolodny et al, 2020).…”

Section: Microbiome and Behavioral Traitsmentioning

confidence: 99%

Domestication and microbiome

et al. 2021

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In this paper we discuss two universal characteristics of domesticated species that distinguish them from the wild closely related ancestors – increased socialization and phenotypic variability. Examining evidence accumulated in the literature up to date, we note that the gut microbiome is involved in the increased social behavior of domesticated species through the gut-immune system-brain axis. We further discuss data that point toward clear difference in the microbiome composition between domesticated species and closely related wild ancestors. This difference is related to changes in diet, due to co-habitation with humans, which leads to increase in Bifidobacteria and changes in carbohydrate metabolism. We note that these changes may also influence interaction between microbiome and virome. Virome is linked to the evolutionary changes through incorporation of retro-viruses into the host genome. Together with transposons these mobile genetic elements may also lead to changes in regulatory networks, and increase adaptive potential. Changes in microbiome of animals during co-habitation with humans should be considered as an important event during domestication process.

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The role of the microbiome in host evolution

Cited by 39 publications

References 16 publications

Immunogenetic Variation Shapes the Gut Microbiome in a Natural Vertebrate Population

Immunogenetic Variation Shapes the Gut Microbiome in a Natural Vertebrate Population

Microbe‐mediated adaptation in plants

Domestication and microbiome

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