Ecological drivers of the evolution of symbiosis

Beneficial symbioses are widespread in nature and underpin the function of both natural and manmade ecosystems. Moreover, by providing the interacting species with new ecological functions, symbiosis represents an important source of innovation and has thus played a crucial role in the evolution of life on Earth.

Although beneficial symbioses are important, their evolution is hard to explain because it requires for once independent species to overcome their self-interest and become an integrated organism. A simple but so far untested idea for how stable beneficial symbioses might evolve is that they start off as exploitative interactions, wherein the host organism captures and exploits their symbiont for the beneficial function they provide.

If the environment inside the host is sufficiently different to that experienced outside the host, the symbiont will over time adapt to this new niche and in so doing lose their ability to thrive outside the host due to trade-offs between the different traits required to survive in each environment. Through this process, the fitness interests of the host and symbiont species become aligned such that each now relies upon the other.

Testing this idea in most symbiotic interactions is impossible because they originated millions of years ago and now the species cannot be separated to test for adaptation to free-living environments.

In this project we overcome this challenge by using an experimentally tractable microbial symbiosis between the single-celled ciliate host Paramecium and the green alga Chlorella, which can either live inside the host cell (intracellular niche) or live freely in freshwater (extracellular niche). We will sample free-living and symbiotic algal populations from UK lakes, and compare their adaptation to key environmental parameters predicted to vary between the intracellular and extracellular niches.

Using comparative genomics we will identify the patterns of genome divergence between the symbiotic and free-living algae and identify genetic adaptations to the symbiotic and free-living lifestyles. Finally, we will experimentally evolve symbiotic algae in the laboratory under free-living environmental conditions to test if this leads to the loss of their symbiotic ability through trade-offs.

Together these experiments will advance our understanding of the biology of symbioses, helping to solve the long-standing evolutionary puzzle of how and why symbioses originate and evolve. In so doing the research will also provide insight into how symbioses and the important functions they perform can be maintained in natural and man-made ecosystems.