Evolution and ecology of phenotypic plasticity in parasite life history strategies

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

The environments experienced by parasites inside hosts and vectors are highly changeable. For example, resources become scarce as hosts get sick, immune responses directed at parasites develop, and parasites often have to compete with other strains and species sharing their host. Given that parasites live in the bodies of others, with which they are engaged in a life-and-death struggle, knowledge about how parasites cope with the challenges of their lifestyle is remarkably shallow.

Understanding the strategies that parasites have evolved to cope with the challenging environments they face inside hosts and vectors is the aim of this proposal. Parasite strategies are important because they are determinants of how sick hosts get (virulence) and how infectious parasites are (transmission). In evolutionary ecology, plasticity in life-history traits is a well-known adaptation to life in variable environments. Adaptive plasticity enables organisms to change their phenotype in response to changes in their circumstances in ways that maintain fitness across environments. That the environment is complex and shapes phenotypes has been known for over a century but because parasites have been viewed as creatures with inflexible strategies, plasticity in their traits - and whether it is beneficial - has been overlooked.

Mounting evidence is revealing considerable plasticity in parasite traits that underpin the ability to survive during infections and to transmit to new hosts. Our recent research shows that parasites adjust their traits in response to the conditions (resource availability, competition with other strains, and anti-parasite drugs) they experience in the host. We know want to investigate why parasites do this by testing theory that predicts they adjust their traits in ways that maximise fitness. We will identify how much variation in parasite traits is explained by parasite strategies and complex interactions between hosts and parasites, whether plasticity benefits parasites, and whether plasticity has evolved to enable to parasites to cope with variable environmental conditions. Therefore, our project will reveal how sophisticated parasite strategies for survival and transmission really are, and reveal weaknesses that could be exploited for disease control.

Malaria (Plasmodium) parasites offer an excellent system to explain the ecological and evolutionary drivers of variation in traits that shape the virulence and transmission phenotypes of parasites. A key fitness-determining trait for malaria parasites is the trade-off between the allocation of resources to asexually replicating stages (required for within-host survival) and sexually reproducing stages (required for transmission), which is called "reproductive effort" in evolutionary biology. Our project will determine how host and parasite factors contribute to plasticity in reproductive effort, quantify the patterns generated across environmental gradients and parasite genetic backgrounds, test whether parasite strategies are adjusted in response to the environment in ways that benefit survival and transmission, and investigate whether plasticity is costly by testing if it is lost under selection in constant environmental conditions.

Explaining variation in the virulence and infectiousness of parasites is a major aim in evolutionary biology and predicting how parasites adapt to their environment is becoming increasingly important. For example, changes in parasite ecology (e.g. composition of host-parasite-vector communities, and habitats) are implicated in the emergence of new infectious diseases of wildlife, crops, livestock, and humans. For applied science, a better understanding of parasites is necessary because evolution continually erodes efforts to control diseases responsible for considerable mortality and morbidity.

Planned Impact

In addition to the academic beneficiaries described above, our research will also benefit the following groups.

PUBLIC. We have strong track records in communicating with the media (for recent efforts see http://reece.bio.ed.ac.uk/media.html) and write press releases on our work. We will continue to seek these opportunities and contribute to local science festivals, public engagement events, and participate as experts in online discussions.

HIGH SCHOOL PUPILS. We will organize an event for sixth form Biology students to visit our lab, learn about and observe our research, and talk to lab members in an informal setting. The ambitions for this event also include an opportunity to communicate to students what evolutionary biology and ecology can bring to all biological disciplines.

POLICY MAKERS AND DRUG DEVELOPERS INVOLVED IN DISEASE CONTROL. Our project will use evolutionary theory to understand how parasites adapt to maximize in-host survival and between-host transmission. Whilst we focus on malaria parasites, the fitness components we study are general to all sexually reproducing organisms so our results will be relevant to a broad range of infectious disease researchers. The information we generate will ultimately inform the development of intervention strategies that interfere with transmission, including the potential for new types of drugs. Because members of these communities usually have a biomedical background, communicating the value of an evolutionary framework for disease control is a task for evolutionary ecologists. We will organise a workshop to communicate the short- and long-term implications of our project to relevant users and explore what directions for the development of our project would be most useful to users. We will use established contacts with policy makers, field and clinical parasitologists, and biomedical researchers to form the participants list. In our experience these groups are curious about what an evolutionary framework can offer to disease control, but clear links between experimental data and pathogenicity or epidemiology are required to turn passing curiosity into sufficient interest to engage in knowledge transfer. We will also use this workshop to form collaborations to test our key results in natural populations and to improve procedures to monitor markers for parasite evolution in natural populations.

The benefits of our research to the above groups will also be facilitated by developing a website with an area dedicated to the provision of information targeted to professional users and a parallel area to communicate to the media and public by outlining the rationale and objectives of the project and lay translations of all resulting papers.

Publications

10 25 50
 
Title ASCUS art exhibition 
Description ASCUS-CIIE microresidencies. 4 artsists created an exhibition based on science from the department including ours. Various lab members were involved. The exhibition "transmissions" was presented in various Scottish venues. The exhibition included artwork as well as film (featuring several lab members) 
Type Of Art Artwork 
Year Produced 2014 
Impact Inspiring collaboration with the artists involved, plus reaching a large audience through the exhibition of their work. 
URL http://www.ascus.org.uk/the-micro-residency-begins/
 
Description Malaria parasites plastically adjust reproductive effort in response to stressful in-host conditions including drugs and competition. Parasites detect and respond to changes in their in-host environment in the manners predicted by evolutionary theory. Our data enabled us to identify some of the cues parasites use for such responses.
Exploitation Route Development of treatment regimes (e.g. dosing strategies) that are tailored to parasite populations and take into the account of how drugs and in-host ecology interact to influence disease severity and transmission.

Development of novel drugs that "trick" parasites into making suboptimal decisions for their fitness.
Sectors Education,Healthcare,Pharmaceuticals and Medical Biotechnology

URL http://reecelab.science/
 
Description placements and work experience for school students; ASCUS art exhibition, Edinburgh Science festival 2015, activites in local schools from nursery to secondary level, yearly School of Biological Sciences open days and media coverage
First Year Of Impact 2013
Sector Education,Leisure Activities, including Sports, Recreation and Tourism,Culture, Heritage, Museums and Collections
Impact Types Cultural,Societal

 
Description Wellcome Trust - Investigator Award
Amount £1,527,986 (GBP)
Funding ID WT/202769/Z/16/Z 
Organisation Wellcome Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 03/2017 
End 03/2022
 
Description NERC2012 collaborations 
Organisation University of Toronto
Country Canada 
Sector Academic/University 
PI Contribution Discussion and data exchange to optimise their mathematical model to quantify reproductive effort
Collaborator Contribution early access to the mathematical model developed by mideo's groups and optimisation of that model for our specific research goal
Impact currently using the model developed by mideo's group - outputs include 2018 PLoS Pathogens paper
Start Year 2012
 
Description ASCUS art exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact ASCUS-CIIE microresidencies. 4 artsists created an exhibition based on science from the department including ours. Various lab members were involved. The exhibition "transmissions" was presented in various Scottish venues.
Year(s) Of Engagement Activity 2014
URL http://www.ascus.org.uk/the-micro-residency-begins/
 
Description Conference-BSP2015-Char 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact presentation of research to academics, British Society Parasitolgoy. Poster by Charlotte Repton
Year(s) Of Engagement Activity 2015
 
Description Conference-BSP2015-PS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact presentation of research to academics
Year(s) Of Engagement Activity 2015
 
Description Conference-Biomalpar2013-PS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact presentation of research to academics, Biomalpar conference in Heidelberg Germany. Poster
Year(s) Of Engagement Activity 2013
 
Description Departmental seminar invitations 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Other audiences
Results and Impact Invited departmental seminar presentations (1-3 per year). Presentation of scientific results to academics.
Year(s) Of Engagement Activity 2007,2008,2009,2010,2011
 
Description Dept.talk-Liverpool2013-PS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact invited presentation of research to academics
Year(s) Of Engagement Activity 2013
 
Description Dept.talk-Paisley2014-PS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact invited presentation of research to academics
Year(s) Of Engagement Activity 2014
 
Description Edinburgh International Science Festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Research exhibition at the Edinburgh science festival.
Year(s) Of Engagement Activity 2015
 
Description Intl_Keynotes_SR 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Invited keynote presentations _ international (1-3 per year). Presentation of scientific results to academics.
Year(s) Of Engagement Activity 2010,2011,2012,2013,2014
 
Description Natl_Keynotes_SR 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other audiences
Results and Impact Invited keynote presentations _ national (1-3 per year). Presentation of scientific results to academics.
Year(s) Of Engagement Activity 2006,2007,2008,2009,2010
 
Description University Doors open day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Open day and undergraduate open day (simultaneous). Display about our research on mosquitoes and malaria
Year(s) Of Engagement Activity 2015,2016,2017
 
Description conference-BSP2013-PS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact presentation of research to academics
Year(s) Of Engagement Activity 2013
 
Description exhibits in primary and secondary schools 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact visits to schools and visits of students to our lab to learn about our research
Year(s) Of Engagement Activity 2012,2013,2014,2015,2016
 
Description nursery school activity - mosquitoes 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact development of activity for young children - teaching them about mosquitoes. 23 children attended, looked at various life stages using microscopes, asked questions and then made an art exhibition about mosquitoes.
Year(s) Of Engagement Activity 2014,2015,2016
 
Description podcast 'naked scientists' about plos pathogens paper 2018 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact podcast 'naked scientists' about plos pathogens paper 2018.
Year(s) Of Engagement Activity 2018
URL https://www.thenakedscientists.com/podcasts/short/modelling-malaria
 
Description press coverage 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact We have strong track records in communication with the media and contribute press releases on our work.
Year(s) Of Engagement Activity 2008,2009,2010,2011,2012
 
Description press release plos pathogens paper 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact press release on the Plos Pathogens 2018 paper. Picked up by the National, and various national and international science websites
Year(s) Of Engagement Activity 2018
 
Description school visit 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact participation in local primary school science event. Our interactive exhibit was very popular. 5 P5 and P6 classes visited.
Year(s) Of Engagement Activity 2018