Ecological drivers of evolutionary transitions in mutualistic symbioses

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences


Intimate and prolonged associations between different organisms - symbioses - are widespread and important in the natural environment. A key form of symbiosis are associations involving photosynthetic organisms which provide their hosts with energy from sunlight: so called photosymbioses. Examples of photosymbioses include lichens, where a fungus hosts an green alga, and corals, where a cnidaria hosts a zooxanthellae alga. Through photosymbiosis pairs of organisms can survive in environments where neither would alone, therefore photosymbioses increase biodiversity and underpin the functioning of ecosystems. An important feature of photosymbiosis is that the benefits to hosts of carrying symbionts depend upon the environmental conditions: for instance in well-lit habitats symbionts are highly beneficial to hosts whereas in dark environments symbionts may be costly for hosts to maintain. Here, we want to understand how environmental variation in light intensity shapes the long-term evolution of photosymbioses.

Despite their widespread importance, little is known about the evolutionary origins of photosymbioses. Possible reasons for this are that lichens and corals are ancient associations and are very slow growing and hard to cultivate in the lab. Our approach is to observe the real-time evolution of a photosymbiosis created by us in the lab between a single-celled eukaryote host (Paramecium) and a photosynthetic cyanobacteria symbiont (Synechocystis). Although many Paramecium-alga symbioses exist in nature, by using a 'synthetic' symbiosis we will capture the entire evolutionary history of the symbiosis from the moment of its inception. We will exploit the short generation times, and large population sizes of Paramecium to observe evolution in real time for 100s of generations. We will discover and contrast the adaptations of both hosts and symbionts that occur as they co-evolve across a gradient of light intensity from near dark to bright light. To fully understand the physiological, biochemical and genetic bases of adaptations we will employ cutting edge cell-imaging, mass spectrometry and genome sequencing technologies.

- Our study is novel because we will, for the first time, study the evolution of a photosymbiosis from inception for 100s of generations in real time
- Our study is relevant to the natural environment because we test the effect of environmental variation of a crucial ecological variable affecting photosymbioses: light intensity. Moreover, our findings will help to predict responses of natural photosymbioses to changing environments
- Our study is powerful because we will use an experimental approach to study evolution in real time.
- Our study is timely because we will exploit the latest technologies in DNA sequencing, biochemistry and cell-imaging to directly observe evolution of genetic, physiological and biochemical adaptations.

Planned Impact

This is blue-skies research that is unlikely to be of immediate and direct industrial or clinical impact within the 3-years of the project. Therefore, despite the potential for industrial collaboration in the future (e.g., biofuels), it would be premature to involve industrial or policy partners at this early stage. Nevertheless we will, over the course of the project, engage with applied microbiologists to discuss concepts of symbiosis and coevolution to the field through presenting our ideas and findings at microbiology and protistology meetings (e.g., Society for Applied Microbiology Conference), and by giving seminars at applied research institutes (e.g., FERA, York).

We envisage that the main impact activities associated with our project will be directed towards improving public understanding of science. In particular, we believe that experimental evolution research has an important role to play in furthering public understanding of key concepts in evolution because the rapid evolutionary rates of these systems mean that actual evolutionary change can be observed in real time. Specifically, Lowe will perform 2 school visits per year facilitated by the National STEM Centre based at the National Science Learning Centre, University of York. In years 1 & 2 of the project, visits will comprise a presentation and group activities aimed at improving the students' grasp of evolution (e.g., natural selection card games), in year 3, we will introduce simple practical classes whereby, over 2 sessions, students will observe the outcomes of symbiosis before their eyes. The classes will utilise the natural symbiosis system Paramecium-Chlorella: First, students will observe using microscopes "white" aposymbiotic Paramecium and "green" holobiont Paramecium. Second, students will grow cultures of "white" and "green" Paramecium in the light and in the dark and measure growth rates to quantify the costs and benefits of symbiosis. Students will learn about the key role of symbiosis in natural ecosystems (e.g. coral reefs, lichens) and how symbiosis underpins the evolution of organelles.

Another important mode of public engagement is Sci-Art collaboration. Interactive performances are the ideal medium for public engagement, as they can communicate scientific concepts in a non-verbal and entertaining way for all age groups. Brockhurst has a track record of involvement in projects and workshops with practicing artists, where his role has been to communicate cutting-edge scientific concepts. Here we propose a sci-art project to enhance public understanding of symbiosis in the evolution of life in collaboration with the UK-based French artist Laurence Payot. Payot mixes visual art with live performance and audience participation. Payot has collaborated on educational projects with numerous schools and communities and delivered large family projects for Tate Liverpool and Liverpool Biennial of Contemporary Art. She has created commissioned artworks for prestigious international galleries and museums including Tate Modern. The proposed activity, "Symbiosis: Social experiments with living sculptures", will use participatory visual art to actively engage with a general audience and demonstrate the important role of symbiosis in the evolution of life and biodiversity. The works will replicate, in a metaphoric way, the relationship between host and endosymbiont in the symbiotic relationship, using sculptures as a host, and the participating audience as the endosymbiont. A series of 'sculptures to wear' will become hosts for human bodies, only existing as living sculptures while populated by their guests, to return to empty shells when the bodies have gone. The sculptures will be toured in various locations in Yorkshire where they will be activated by different types of communities (from primary schools to football crowds).


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Related Projects

Project Reference Relationship Related To Start End Award Value
NE/K011774/1 31/03/2014 01/01/2017 £396,899
NE/K011774/2 Transfer NE/K011774/1 02/01/2017 01/04/2017 £23,697
Description SEE MAIN REPORT FOR THIS GRANT FOR THE PUBLICATIONS; UNABLE TO UPLOAD HERE DUE TO PUBLICATION DATES PRECEDING THE START DATE OF THE MOVED AWARD. We have shown using experiments with the Paramecium-Chlorella photo-symbiosis that the basis of its stability is exploitation of the symbiont by the host. This provides the first direct empirical evidence in support of longstanding theory that evolutionarily stable symbiosis can result from partner control and exploitation rather than mutualism. Published in Current Biology (2016). We have developed mathematical models of the physiological and ecological mechanisms of symbiosis allowing our findings to be generalised to a wide range of ecologically important symbioses. Published in Journal of Theoretical Biology and Royal Society Open Science (2016). We have completed experiments showing natural variation in the dependence host-symbiont genotypes. Published in BMC Evolutionary Biology (2018). We have shown using metabolomics that independent evolutionary origins of this symbiosis use a convergent nutrient exchange but concurrently have diverged in secondary symbiotic traits; this facilitates partner-switching and allows hosts to aqcuire new phenotypic traits. Published in Current Biology (2020). Further experiments show that mismatched partner-switched symbioses can rapidly evolve to attain higher fitness stabilising the symbiosis (1 manuscript in preparation).

We have also published, a review of the literature on the contribution of biotic conflicts to evolution (Brockhurst et al. 2014 Proceedings of the Royal Society B) and the role of exploitation in the establishment of symbiosis, published in FEMS Microbiology Letters (2019).
Exploitation Route Future grants will address the role for extrinsic ecological drivers such as predation and variable resource supply on the evolution of stability in symbioses
Sectors Environment

Description The research fed into public engagement activity: a collaboration with artist Laurence Payot, LIVING SCULPTURES, about symbiosis which involved over 200 participants making sculptures and was displayed to public audiences at York Festival of Ideas 2014, Sheffield Festival of the Mind 2014, The Bluecoat Gallery Liverpool in 2015, York Art Gallery in 2017, TATE Liverpool in 2017, and public spaces across East Cheshire as part of SHIFT; total audience approx. 15000, funded by grants from Arts Council England and The Wellcome Trust and providing 100 days of employment for artists
First Year Of Impact 2017
Sector Creative Economy,Education,Leisure Activities, including Sports, Recreation and Tourism,Culture, Heritage, Museums and Collections
Impact Types Cultural,Societal

Description SHIFT a touring art exhibition in public spaces in Cheshire East 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Living Sculptures Virtual was shown in public places throughout Cheshire East in 2017/2018 and has been interacted with by 100s of members of the general public
Year(s) Of Engagement Activity 2017,2018
Description TATE Exchange (TATE Liverpool) - The Alchemy Between Us 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Living Sculptures were exhibited to the public and a public lecture was delivered entitled "The Alchemy Between Us: Making Sense of the World" at Tate Liverpool 11-17 Dec 2016
Year(s) Of Engagement Activity 2016