An agent-based model of adaptation of holobionts with different microbial symbiont transmission modes

Abstract

The hologenome theory suggests that holobionts (host plus symbiont) with hosts that are only able to adapt slowly may be able to persist in deteriorating environmental conditions via rapid adaptation of their microbial symbionts. The effectiveness of such symbiont adaptation may vary depending on whether symbionts are passed directly to offspring (vertical transmission) or acquired from the environment (horizontal transmission). However, it has been suggested that holobionts with horizontal transmission cannot pass down their symbionts faithfully, preventing adaptation at the holobiont level because of host-symbiont disassociation between generations. Here we used an agent-based model to investigate whether holobionts with horizontal microbial symbiont transmission can adapt to increasing stress solely through symbiont adaptation and compared their adaptation to holobionts with vertical transmission. We found that holobionts with either transmission mode were able to adapt to increasing abiotic stress solely via symbiont adaptation. Moreover, those with horizontal transmission were more competitive than those with vertical transmission when hosts were able to selectively associate with the most suitable symbionts. However, those with horizontal transmission were less competitive than those with vertical transmission when symbiont establishment was random. Our results support the hologenome theory and demonstrate that holobionts with horizontal microbial symbiont transmission could adapt to increasing abiotic stress via their symbionts. We also showed that whether holobionts with horizontal or vertical symbiont transmission are favored in increasingly stressful conditions depends on the ability of hosts to recognize and foster microbial symbionts that confer stress tolerance. IMPORTANCESymbiotic organisms such as reef building corals are sensitive to environmental perturbations due to anthropogenic disturbances or climate change, and it is critical to understand whether they are able to adapt to previously unfavorable conditions. To date, studies have focused on the impacts of existing microbial symbiont variation on holobiont stress tolerance but here we use agent-based models to explore holobiont adaptation via symbiont adaptation. We studied both deterministic and stochastic processes in holobiont adaptation by investigating the following four factors: holobiont transmission modes, a hosts ability to recognize tolerance-conferring symbionts, a symbionts mutational variance, and rate of stress increase. Our simulation provides a comprehensive understanding of holobiont adaptation under stress, which not only has implications for future endangered symbiotic species management, but also provides fresh insight into species evolution as proposed by the hologenome theory.