Within-host microbial selection and multiple microbial generations buffer the loss of host fitness under environmental change.

Abstract

The relationship between, and joint selection on, a host and its microbes-the holobiont-can impact evolutionary and ecological outcomes of the host and its microbial community. We develop an agent-based modelling framework for understanding the ecological dynamics of hosts and their microbiomes. Our model incorporates numerous microbial generations per host generation allowing selection on both host and microbes. We then explore host and microbiome fitness and diversity in response to environmental change. We demonstrate that multiple microbial generations can buffer changes experienced across host lifetimes by smoothing environmental transitions. Our simulations reveal that microbial fitness and host fitness are at odds with each other when considering the impact of vertical inheritance of microbial communities from a host to its offspring-where high parent-offspring microbial transmission favours microbial fitness, while low transmission favours host fitness. These tradeoffs are minimized when microbial generation count per host generation is high. This may arise from 'cross-generational priority effects' which maintain diversity within the community and can subsequently enable selection of beneficial microbes by the host. Our model is extensible into new areas of holobiont research and provides novel insights into holobiont evolution under variable environmental conditions.