Doctoral defense by Elena Horas

The effects of symbiotic interactions on the ecology and evolution of the alga Chlorella variabilis

Abstract

Our planet’s biodiversity is made up of a wide array of species interactions that vary in strength and direction. Species interactions make up biological communities and ecosystems and they are crucial for the evolution and diversification of species. Well known examples include the evolution of eukaryotic cells from endosymbiotic interactions between two prokaryotic cells or the divergence of hosts due to cycles of antagonistic coevolution with their parasites. Even though studying the causes and consequences of the evolution of species interactions has been a central focus of research for several decades, understanding how it unravels within complex biotic environments remains largely unexplored.

In this thesis, I studied how the biotic context can affect the ecology and evolution of symbiotic interactions. I worked with the unicellular freshwater alga Chlorella variabilis studying its multiple and different interactions with other species. In one of my chapters, I focused on Chlorella variabilis and its interaction with the ciliate Paramecium bursaria, with which they form a mutualistic endosymbiotic interaction. Specifically, I investigated the costs and benefits of this interaction to the endosymbiotic algae and to its ciliate partner by comparing their fitness in symbiosis with their fitness when free-living along changing biotic environments. I found that both, endosymbionts and hosts, benefitted from the interaction due to the predatory activity that the ciliates have on free-living Chlorella. These results suggest that the current mutualism between the two species might have evolved from an initial antagonistic interaction. Within another chapter, I investigated the antagonistic interaction between Chlorella variabilis and its lytic chlorovirus PBCV-1. I found that coexistence of both species was possible due to a coevolutionary arms race in which each species increased their ability to either resist or infect over time. Interestingly, these dynamics were impeded when the ciliate Paramecium bursaria was present. Under this scenario, the alga evolved resistance, but the virus was unable to counter-adapt. Further experimental evidence showed that these differences in the algae-virus coevolutionary dynamics could be due to the combination of different algal resistance mechanisms, lower density of viral particles and higher frequency of susceptible algal cells in the presence of ciliates. Finally, one of the chapters consisted of a literature review where I identified the ecological conditions, divided into intrinsic and extrinsic factors, that render algal viruses unsuccessful in completing their life cycles. This chapter was complemented with diverse examples and analyses of experimental data. Overall, this thesis provided evidence that the evolution of species interactions can change in direction (i.e., from antagonistic to mutualistic) and strength (i.e., from arms race coevolution to no coevolution) depending on the biotic context. It thus highlighted the importance of studying species interactions within more complex communities.