Joint consideration of selection and microbial generation count provides unique insights into evolutionary and ecological dynamics of holobionts

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. Here we present a novel agent-based modelling framework for understanding the ecological dynamics of hosts and their microbiomes. Our model explicitly incorporates numerous microbial generations per host generation allowing for selection on both host and microbe. We apply our model to explore community fitness and diversity in the face of rapid 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 may be at odds with each other when considering the impact of vertical inheritance of microbial communities from a host to its offspring - where high values favour microbial fitness, while low values favour host fitness - these tradeoffs are minimized when microbial generation count per host generation is high. We suggest that these results arise from 'cross-generational priority effects' which maintain diversity within the community and can subsequently be acted upon by selection. Our model is readily extensible into new areas of holobiont research and provides novel insights into holobiont evolution under variable environmental conditions.