Gut microbiome heritability is nearly universal but environmentally contingent

Abstract

Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

Feed and Host Genetics Drive Microbiome Diversity with Resultant Consequences for Production Traits in Mass-Reared Black Soldier Fly (Hermetia illucens) Larvae

“…Recent studies have instigated a paradigm shift regarding our understanding of the fundamental principles that govern the diversity of complex gut ecosystems, advocating for a more pronounced influence of host genetics than previously thought [78]. While these effects are most evident at evolutionary scales [79,80], patterns of co-segregation between host genetic and microbiome factors in human, murine, and swine models highlight that substantial individual-level heritability in animal GIT microbial landscapes can be anticipated [81][82][83][84][85]. Herein, it is expected that the studied larval cohorts are genetically distinct as BSF populations experience large decreases in genetic variation and rapid generational differentiation in closed mass-rearing systems [21].…”

“…Quantitative genetics studies have described putative determinants underlying patterns of microbiome heritability, commonly ascribing host-mediated control of gut community assemblages to genes of the immune system [29,30,85,86] and metabolic [87] pathways. Furthermore, it has been illustrated that microbiome-host dynamics may be highly complex and governed by a variety of polygenic, pleiotropic, or even environment-interactive genetic mechanisms [86,[88][89][90].…”

You are more than what you eat: potentially adaptive enrichment of microbiome functions across bat dietary niches

“…A major caveat of this approach is that microbiome functions need to be heritable to be considered as traits of the host. Current evidence for vertical transmission is lacking for mammals, but there is some evidence that wild animals have a higher proportion of heritable gut bacteria than previously thought [ 45 ]. Given that the gastrointestinal traits governing this filter have a genetic, and therefore potentially heritable, basis [ 46 ], we also suggest that some microbiome members may be considered as “functionally inherited” if microbial metabolites, rather than species, are the actual targets of host selection [ 47 ].…”

AMDB: a database of animal gut microbial communities with manually curated metadata

“…In particular, host phylogeny and diet largely account for the gut microbiota variations ( 7 ). A recent analysis of samples from wild baboons found widespread gut microbiome heritability ( 9 ). This vertical transmission may be one of the drivers of phylosymbiosis ( 10 ).…”