Metabolic mechanisms for the evolution of stable symbiosis

Endosymbiosis involves the merger of once independent organisms; this evolutionary transition has defined the evolutionary history of eukaryotes and continues to underpin the function of a wide range of ecosystems. Endosymbioses are evolutionarily dynamic because the inherent conflict between the self-interest of the partners make the breakdown of the interaction ever-likely and this is exacerbated by the environmental context dependence of the benefits of symbiosis. This necessitates selection for partner switching, which can reshuffle the genetic identities of symbiotic partnerships and so rescue symbioses from cheater-induced extinction and enable rapid adaptation to environmental change. However, the mechanisms of partner-specificity, that underlie the potential for partner switching, are unknown. Here I report the metabolic mechanisms that control partner specificity within the tractable microbial photosymbiosis between Paramecium bursaria and Chlorella . I have found that metabolic function, and not genetic identity, enables partner-switching, but that genetic variation plays an important role in maintaining variation in symbiotic phenotype. In addition, I observed that symbiont stress-responses played an important role in partner specificity, and that alleviating symbiont stress responses may be an important strategy of generalist host genotypes. Furthermore, I have used experimental evolution to show that a novel, initially non-beneficial association can rapidly evolve to become a beneficial symbiosis. These results demonstrate that partner integration is defined by metabolic compatibility and that initially maladapted host-symbiont pairings can rapidly evolve to overcome their lack of co-adaptation through alterations to metabolism and symbiont regulation. Understanding the process of novel partner integration and partner switching is crucial if we are to understand how new symbioses originate and stabilise. Moreover, mechanistic knowledge of partner switching is required to mitigate the breakdown of symbioses performing important ecosystem functions driven by environmental change, such as in coral reefs