The microbiome extends host evolutionary potential

Abstract

The microbiome shapes many host traits, yet the biology of microbiomes challenges traditional evolutionary models. Here, we illustrate how integrating the microbiome into quantitative genetics can help untangle complexities of host-microbiome evolution. We describe two general ways in which the microbiome may affect host evolutionary potential: by shifting the mean host phenotype and by changing the variance in host phenotype in the population. We synthesize the literature across diverse taxa and discuss how these scenarios could shape the host response to selection. We conclude by outlining key avenues of research to improve our understanding of the complex interplay between hosts and microbiomes.

Population bottlenecks constrain host microbiome diversity and genetic variation impeding fitness

“…Despite recent calls for an integration of microbiome research in evolutionary and conservation biology [ 18 , 21 , 22 , 27 , 28 , 36 , 46 , 47 ], little progress has been made on experimentally testing fundamental associations between population size, host genetic variation and microbial diversity. Here we provide a novel demonstration that restricting host population size has a profound impact on both the richness and the diversity of host-associated microbiomes, and that effects of host genetic variation and microbial richness interact synergistically in affecting host fitness.…”

“…According to the hologenome hypothesis, the holobiont constitutes a single unit of selection, thus our results suggest that small and fragmented populations have a reduced potential for responding to selection pressures not only due to reduced genetic variation and high rates of inbreeding but also due to reduced microbiome variation, effectively reducing hologenomic variation. Maintaining a diverse microbiome community may therefore be crucial for a host’s responsiveness to environmental change [ 22 – 24 , 42 ].…”

“…Because interactions between microbes and their hosts shape so many aspects of life, the impact on core biological processes including evolutionary adaptation may need to be reconsidered [ 19 – 22 ]. The ‘holobiont’ concept reflects the idea that eukaryote individuals do not act as autonomous units, but rather as networks consisting of the host and all its associated microbiota, and that their collective genomes–the ‘hologenome’–forms a cohesive unit of selection [ 23 – 25 ].…”

“…We hypothesise that reduced host genetic variation provides a less diverse environment for microbes leading to reduced microbial diversity through fewer host genotype-microbial taxon-specific interactions ( Fig 1 ). Evidence suggests that increased microbiome diversity is adaptive for the host and that increased hologenome genetic variation facilitates faster evolutionary responses to selection [ 22 , 25 , 36 ]. Our work further highlights the importance of considering both host and microbiome diversity for predicting evolutionary consequences of population bottlenecks in small and threatened populations.…”

Anthropogenic disturbance impacts gut microbiome homeostasis in a Malagasy primate

“…However, more resilient species might also suffer from human encroachment, especially if this disturbs the host-gut microbiome (Fackelmann et al 2021). Now known as an important component of health, the gut microbiome provides several necessary services to its host, ranging from nutrition uptake and metabolism to the shaping of immunity, disease resistance and behaviour and its overall support of the host's adaptation to various environment conditions (Thomas et al, 2017;McKenney et al, 2018;Fackelmann et al, 2021;Henry et al, 2021). The gut microbiome itself is shaped by several intrinsic (i.e.…”