Bruijning, M. | Search bioRxiv

bioRxiv2020

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

The microbiome can contribute to variation in fitness-related traits of their hosts, and thus to host evolution. Hosts are therefore expected to be under selection to control their microbiome, for instance through controlling microbe transmission from parents to offspring. Current models have mostly focused on microbes that either increase or decrease fitness. In that case, host-level selection is relatively straightforward, favouring either complete or no inheritance. In natural systems, however, vertical transmission fidelity varies widely, and microbiome composition is often shaped by a combination of vertical and horizontal transmission modes. We propose that such mixed transmission could optimize host fitness under fluctuating environments. Using a general model, we illustrate that decreasing vertical transmission fidelity increases the amount of microbiome variation, and thus potentially phenotypic variation, across hosts. Whether or not this is advantageous depends on environmental conditions, how much the microbiome changes during host development, and the contribution of other factors to trait variation. We discuss how environmentally-dependent microbial effects can favor intermediate transmission, review examples from natural systems, and suggest research avenues to empirically test our predictions. Overall, we show that imperfect transmission may be adaptive by allowing individuals to ensure phenotypic variability in their offspring in contexts where varying environments mean that this strategy increases long-term fitness.

evolutionary biology↗

bioRxiv2019

Can the microbiome influence host evolutionary trajectories?

The microbiome shapes many traits in hosts, but we still do not understand how it influences host evolution. To impact host evolution, the microbiome must be heritable and have phenotypic effects on the host. However, the complex inheritance and context-dependence of the microbiome challenges traditional models of organismal evolution. Here, we take a multifaceted approach to identify conditions in which the microbiome influences host evolutionary trajectories. We explore quantitative genetic models to highlight how microbial inheritance and phenotypic effects can modulate host evolutionary responses to selection. We synthesize the literature across diverse taxa to find common scenarios of microbiome driven host evolution. First, hosts may leverage locally adapted microbes, increasing survivorship in stressful environments. Second, microbial variation may increase host phenotypic variation, enabling exploration of novel fitness landscapes. We further illustrate these effects by performing a meta-analysis of artificial selection in Drosophila, finding that bacterial diversity also frequently responds to host selection. We conclude by outlining key avenues of research and experimental procedures to improve our understanding of the complex interplay between hosts and microbiomes. By synthesizing perspectives through multiple conceptual and analytical approaches, we show how microbiomes can influence the evolutionary trajectories of hosts.

evolutionary biology↗