Context-dependent costs and benefits of endosymbiotic interactions in a ciliate-algae system

Abstract

Endosymbiosis, an interaction between two species where one lives within the other, has evolved multiple times independently, but the underlying mechanisms remain unclear. Evolutionary theory suggests that for an endosymbiotic interaction to remain stable over time, births of both partners should be higher than their deaths in symbiosis and deaths of both partners should be higher than their births when living independently. However, experimentally measuring this can be difficult and conclusions tend to focus on the host. Using a ciliate-algal system (Paramecium bursaria host and Chlorella endosymbionts), we estimated the benefits and costs of endosymbiosis for both organisms using fitness measurements in different biotic environments to test under which environmental conditions the net effects of the interaction were positive for both partners. We found that the net effects of harbouring endosymbionts were positive for the ciliate hosts as it allowed them to survive in conditions of low-quality bacteria food. The algae benefitted by being endosymbiotic when predators such as the hosts were present, but the net effects were dependent on the total density of hosts, decreasing as hosts densities increased. Overall, we show that including context-dependency of endosymbiosis is essential in understanding how these interactions have evolved.