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.

Complex third-party effects in theDictyostelium–Paraburkholderiasymbiosis: prey bacteria that are eaten, carried or left behind

“…The fitness effects of symbiotic interactions can change depending on the environment [1][2][3][4][5]. One crucial component of the environment that can affect selection on symbiotic interactions is a third species that interacts with hosts or symbionts [6][7][8][9][10].…”

Complex third-party effects in theDictyostelium-Paraburkholderiasymbiosis: prey bacteria that are eaten, carried, or left behind

“…The fitness effects of symbiotic interactions can change depending on the environment (Bronstein, 1994; Chamberlain et al ., 2014; Horas et al ., 2022; Scott et al ., 2022). One crucial component of the environment that often selects for symbiotic interactions is a third species that interacts with hosts or symbionts (Palmer et al ., 2008; Wendling et al ., 2017; Wood et al ., 2018; Hafer-Hahmann & Vorburger, 2020; Cassidy et al ., 2022).…”

Mutualism on the edge: Understanding the Paramecium–Chlorella symbiosis

“…Each cell, measuring less than 150 μm, is packed with hundreds of intracellular green algae from the genus Chlorella ( Fig 1 ). The endosymbiosis is generally beneficial for both partners [ 1 ]. The algae provide sugar (maltose) and oxygen derived from photosynthesis in exchange for nitrogen, carbon dioxide, and ecologically important protection from predation and viruses [ 2 , 3 ].…”

“…The algal population of P. bursaria are housed in organelles poised for destruction, preserved at the mercy of its benevolent host, or for as long as the host continues to receive the cellular signals of "good" behavior. As fundamentally selfish organisms, the fitness interests of host and symbiont are not aligned [1,10]. In such a scenario, exploitative control of this process allows P. bursaria to regulate algal load to maintain its own fitness interests [10].…”