Characterizing evolution of defense in a tripartite marine symbiosis system using adaptive dynamics

The evolution and maintenance of symbiotic systems remains a fascinating puzzle. While the coevolutionary dynamics of bipartite (host-symbiont) systems are well-studied, the dynamics of more complex systems have only recently garnered attention with increasing technological advances. We model a tripartite system inspired by the marine symbiotic relationship between the alga \emph{Bryopsis} sp., its intracellular defensive bacterial symbiont ``\emph{Candidatus} Endobryopsis kahalalidefaciens", which produces a toxin that protects the alga against fish herbivores, and the sea-slug \emph{Elysia rufescens} \citep{zan2019microbial}, which is not deterred by the toxin. We disentangle the role of selection on different actors within this system by investigating evolutionary scenarios where defense evolves as i) a host-controlled trait that reduces algal reproductive ability; ii) a symbiont-controlled trait that impacts symbiont transmission; and iii) a trait jointly controlled by both host and symbiont. Optimal investment in defensive toxins varies based on the characteristics of the host, symbiont, and sea slug; and evolutionary trajectories are modulated by trade-off shape, i.e., a strongly decelerating trade-off between defense and symbiont transmission can drive symbiont diversification via evolutionary branching. Increasing slug herbivory reduces host investment in defense to favour reproduction, while symbiont investment in defense first declines and then increases as host density declines to the degree that horizontal symbiont transmission is no longer beneficial. Increasing vertical transmission selects for reduced defense by the host when it evolves as a jointly controlled trait, as a result of investment by the symbiont. Our theoretical exploration of the evolution of defensive symbiosis in scenarios involving interactions with multiple herbivores provides a first window onto the origin and maintenance of the \emph{Bryopsis} sp. system, and adds another piece to the puzzle of evolution of symbiotic systems.