Past epidemics as predictors of disease evolution over space and time
Lead Research Organisation:
University of Stirling
Department Name: Biological and Environmental Sciences
Abstract
Past epidemics as predictors of disease evolution over space and time
The Earth's climate is changing: temperatures are rising and freak weather events, such as floods, droughts and heat waves, are becoming more frequent. These changing weather patterns are influencing the spread and severity of many infectious diseases. Pests that blight human crops are spreading polewards at an average rate of two miles a year and diseases of humans are also shifting: dengue outbreaks occur in the USA, and the UK climate is predicted to be suitable for malaria by 2050.
Many of these diseases are occur in epidemics - devastating outbreaks that eventually wane, only to occur again in the future. Epidemics are known to drive evolution in natural host populations: individuals that are susceptible to the infectious parasites are eliminated, leaving behind a more resistant population. However, evolution in the host population can drive counter-evolution in the epidemic-causing parasite population: as the susceptible individuals are eliminated, the parasites that are able to infect the more resistant individuals are favoured by natural selection. This is coevolution. Coevolution is not just driven by epidemics; epidemics are also driven by coevolution. This is because the rate and nature of coevolution determines the genetic makeup of both host and parasite populations, and diseases spread much more slowly, i.e., epidemics are smaller, when host populations are genetically diverse.
Climate change is causing fluctuations in parasite transmission between hosts, often leading to more frequent and severe epidemics. But how do current epidemics influence those of the future? Do warmer temperatures, and the large epidemics that follow, lead to smaller or larger epidemics in the long-term? We currently do not know the answer to this; my proposal seeks to change that.
I will test how ambient temperatures and mixing of hosts and parasites (which often happens as a result of freak weather events such as flooding) influences both coevolution and epidemic severity. What is more, I will do this both in the wild - the natural arena of host-parasite interactions - and in artificial outdoor ponds where the temperature can be experimentally manipulated. In the laboratory, I will also quantify how parasite adaptation to the current host population affects its infectivity and growth on future populations (the offspring of the current hosts). I will examine how epidemics in the first year drive epidemic size and severity in subsequent years. This will allow me to generate models that can predict the severity of future disease outbreaks based on past epidemic information. Ultimately, my aim is to develop tools that better predict the likelihood and severity of disease epidemics in an increasingly variable world.
The Earth's climate is changing: temperatures are rising and freak weather events, such as floods, droughts and heat waves, are becoming more frequent. These changing weather patterns are influencing the spread and severity of many infectious diseases. Pests that blight human crops are spreading polewards at an average rate of two miles a year and diseases of humans are also shifting: dengue outbreaks occur in the USA, and the UK climate is predicted to be suitable for malaria by 2050.
Many of these diseases are occur in epidemics - devastating outbreaks that eventually wane, only to occur again in the future. Epidemics are known to drive evolution in natural host populations: individuals that are susceptible to the infectious parasites are eliminated, leaving behind a more resistant population. However, evolution in the host population can drive counter-evolution in the epidemic-causing parasite population: as the susceptible individuals are eliminated, the parasites that are able to infect the more resistant individuals are favoured by natural selection. This is coevolution. Coevolution is not just driven by epidemics; epidemics are also driven by coevolution. This is because the rate and nature of coevolution determines the genetic makeup of both host and parasite populations, and diseases spread much more slowly, i.e., epidemics are smaller, when host populations are genetically diverse.
Climate change is causing fluctuations in parasite transmission between hosts, often leading to more frequent and severe epidemics. But how do current epidemics influence those of the future? Do warmer temperatures, and the large epidemics that follow, lead to smaller or larger epidemics in the long-term? We currently do not know the answer to this; my proposal seeks to change that.
I will test how ambient temperatures and mixing of hosts and parasites (which often happens as a result of freak weather events such as flooding) influences both coevolution and epidemic severity. What is more, I will do this both in the wild - the natural arena of host-parasite interactions - and in artificial outdoor ponds where the temperature can be experimentally manipulated. In the laboratory, I will also quantify how parasite adaptation to the current host population affects its infectivity and growth on future populations (the offspring of the current hosts). I will examine how epidemics in the first year drive epidemic size and severity in subsequent years. This will allow me to generate models that can predict the severity of future disease outbreaks based on past epidemic information. Ultimately, my aim is to develop tools that better predict the likelihood and severity of disease epidemics in an increasingly variable world.
Planned Impact
Who will benefit from this research?
Worldwide, over 50% of deaths in children under five years old are caused by infectious disease, and plant diseases cause crop losses that amount to 12% of global annual productivity. Our changing climate is also causing shifts in patterns of disease over space and time: West Nile Virus is increasingly common in the USA, and the ranges of crop diseases are moving polewards at an average rate of two miles per year. This research is therefore of wide interest to academic and non-academic sectors.
Findings from this research will be promoted to: academic biologists/agriculturists; educational charities; and to the general public.
How will they benefit from this research?
My research will be disseminated in multiple formats to ensure it is visible to the widest possible audience. It will play a role in:
(1) Driving the academic field of evo-epidemiology.
(2) Helping those in agriculture and aquaculture protect against disease.
(3) Engaging the general public in the scientific process.
(4) Educating students of varying ages in how climate factors can affect disease evolution.
(5) Equipping young scientists with the skills to do good science and to promote that science to audiences beyond academia.
My research asks cutting-edge questions regarding how ecological and evolutionary processes interact to affect disease severity over time. It will therefore fuel further productive research by the academic community. To maximise its influence, this research will be published in high-impact journal publications, which will be freely accessible to academics worldwide (either directly through Open Access journals or via the University of Stirling's online research repository, STORRE); it will also be presented at both national and international academic conferences.
Project findings (in particular those from theme 3) will be used to help those in agriculture and aquaculture predict and manage disease epidemics in their crops/stocks from year to year, aiding in long-term disease management and improving the efficiency of food production.
My research will also be actively promoted to the general public through blog posts and short videos explaining up-to-date findings as they are published; findings will also be promoted using social media and to the conventional media via press releases (from the University of Stirling's Media Relations Office, after consultation with NERC). This will generate a public following of the project. Further, science from this project will be used to make a short film for national television (in collaboration with BAFTA award-winning cinematographer, Alan McLaughlic); it will therefore be transmitted into the homes of people throughout the UK and will have direct cultural impact.
Project findings will play a key role in teaching the principles of evolution and how climate change could affect the severity and spread of disease to students of various ages throughout the world. The National Center for Science Education (a US-based charity) has been involved with the designing of this project, and the project's findings form a key component of freely-available interactive learning resource to teach the principles of evolution and climate change. A key aim is to get students to consider how a changing climate could affect disease evolution and severity. It is therefore of considerable educational worth.
Finally, staff and bursary students will acquire important professional skills that are relevant within and outside academia. The technician will acquire new laboratory skills that should help them progress to other fulfilling employment at the end of the contract. The bursary students will be taught numerous scientific skills; they will also be trained in communicating science verbally and in written form (blogs posts journal publications) form to a wide range of audiences. These are invaluable skills.
Worldwide, over 50% of deaths in children under five years old are caused by infectious disease, and plant diseases cause crop losses that amount to 12% of global annual productivity. Our changing climate is also causing shifts in patterns of disease over space and time: West Nile Virus is increasingly common in the USA, and the ranges of crop diseases are moving polewards at an average rate of two miles per year. This research is therefore of wide interest to academic and non-academic sectors.
Findings from this research will be promoted to: academic biologists/agriculturists; educational charities; and to the general public.
How will they benefit from this research?
My research will be disseminated in multiple formats to ensure it is visible to the widest possible audience. It will play a role in:
(1) Driving the academic field of evo-epidemiology.
(2) Helping those in agriculture and aquaculture protect against disease.
(3) Engaging the general public in the scientific process.
(4) Educating students of varying ages in how climate factors can affect disease evolution.
(5) Equipping young scientists with the skills to do good science and to promote that science to audiences beyond academia.
My research asks cutting-edge questions regarding how ecological and evolutionary processes interact to affect disease severity over time. It will therefore fuel further productive research by the academic community. To maximise its influence, this research will be published in high-impact journal publications, which will be freely accessible to academics worldwide (either directly through Open Access journals or via the University of Stirling's online research repository, STORRE); it will also be presented at both national and international academic conferences.
Project findings (in particular those from theme 3) will be used to help those in agriculture and aquaculture predict and manage disease epidemics in their crops/stocks from year to year, aiding in long-term disease management and improving the efficiency of food production.
My research will also be actively promoted to the general public through blog posts and short videos explaining up-to-date findings as they are published; findings will also be promoted using social media and to the conventional media via press releases (from the University of Stirling's Media Relations Office, after consultation with NERC). This will generate a public following of the project. Further, science from this project will be used to make a short film for national television (in collaboration with BAFTA award-winning cinematographer, Alan McLaughlic); it will therefore be transmitted into the homes of people throughout the UK and will have direct cultural impact.
Project findings will play a key role in teaching the principles of evolution and how climate change could affect the severity and spread of disease to students of various ages throughout the world. The National Center for Science Education (a US-based charity) has been involved with the designing of this project, and the project's findings form a key component of freely-available interactive learning resource to teach the principles of evolution and climate change. A key aim is to get students to consider how a changing climate could affect disease evolution and severity. It is therefore of considerable educational worth.
Finally, staff and bursary students will acquire important professional skills that are relevant within and outside academia. The technician will acquire new laboratory skills that should help them progress to other fulfilling employment at the end of the contract. The bursary students will be taught numerous scientific skills; they will also be trained in communicating science verbally and in written form (blogs posts journal publications) form to a wide range of audiences. These are invaluable skills.
People |
ORCID iD |
| Stuart Auld (Principal Investigator / Fellow) |
Publications
Auld SK
(2016)
Sex as a strategy against rapidly evolving parasites.
in Proceedings. Biological sciences
Auld SK
(2015)
The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms.
in Heredity
Auld SK
(2017)
Parasite transmission in a natural multihost-multiparasite community.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Auld SKJR
(2017)
Simulated climate change, epidemic size, and host evolution across host-parasite populations.
in Global change biology
Auld SKJR
(2017)
Environmental variation causes different (co) evolutionary routes to the same adaptive destination across parasite populations.
in Evolution letters
Dobson AD
(2015)
Insufficient evidence of infection-induced phototactic behaviour in Spodoptera exigua: a comment on van Houte et al. (2014).
in Biology letters
Dobson AD
(2016)
Epidemiological Implications of Host Biodiversity and Vector Biology: Key Insights from Simple Models.
in The American naturalist
Goodman J
(2019)
Variation in chronic radiation exposure does not drive life history divergence among Daphnia populations across the Chernobyl Exclusion Zone.
in Ecology and evolution
Goodman J
(2022)
Radiation-mediated supply of genetic variation outweighs the effects of selection and drift in Chernobyl Daphnia populations.
in Journal of evolutionary biology
Paplauskas S
(2021)
Ecology directs host-parasite coevolutionary trajectories across Daphnia-microparasite populations.
in Nature ecology & evolution
Van Houte S
(2015)
Baculovirus infection triggers a positive phototactic response in caterpillars: a response to Dobson et al. (2015).
in Biology letters
| Description | 1. Using a pair of disease models (for mosquito- and tick-borne disease), we simulated how different types of change in host biodiversity led to either increased or decreased levels of disease in the system (measured as densities of infected vectors, proportion of infected hosts etc.) 2. We have shown how sex allows populations to continually evolve when faced with ever-changing disease. 3. Environment affects disease epidemics. We have demonstrated that higher temperatures drive larger epidemics and affect the nature of host-parasite coevolution with impacts on the long-term health of host populations. |
| Exploitation Route | These models could help understand the spread of vector-borne diseases, e.g., malaria, Zika, Lyme disease. |
| Sectors | Agriculture, Food and Drink,Education,Environment,Healthcare |
| Description | Development of disease models used for undergraduate teaching. Societal engagement with evolutionary biology from press, radio and online media. |
| First Year Of Impact | 2014 |
| Sector | Education |
| Impact Types | Cultural,Societal |
| Title | Data from: Environmental variation causes different (co) evolutionary routes to the same adaptive destination across parasite populations |
| Description | This data file includes the infection data for experiments conducted in Auld & Brand 2017 Evolution Letters. ID denotes the individual jar ID, genotype denotes the name of each host genotype, host type denotes whether the host genotype is sympatric or allopatric to the parasite populations, rep denotes the replicate number, pop.epi.size denotes the integrated prevalence of the epidemic from where the parasite isolate was sampled, prop. infected denotes the proportion of parasite hosts that became infected, control.prop.infected denotes the proportion of hosts exposed to the ancestral parasite isolate that became infected, control.spore.burden denotes the density of spores in hosts infected with the ancestral parasite isolate, spore.burden denotes the density of spores in hosts infected with evolved parasite isolates, change.prop.inf denotes the change in infectivity between evolved parasite isolates and controls and change.spore.burden denotes the change in parasite spore burden between hosts infected with the ancestral and evolved parasite isolates. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2017 |
| Provided To Others? | Yes |
| Impact | Contribution to open access data that can be used to conduct further study. |
| URL | https://datadryad.org/bitstream/handle/10255/dryad.157935/Auld%26BrandDataEvolLetts.csv?sequence=1 |
| Title | Ecology directs host-parasite coevolutionary trajectories across Daphnia-microparasite populations |
| Description | Host-parasite interactions often fuel coevolutionary change. However, parasitism is one of a myriad of possible ecological interactions in nature. Biotic (e.g., predation) and abiotic (e.g., temperature) variation can amplify or dilute parasitism as a selective force on hosts and parasites, driving population variation in (co)evolutionary trajectories. We dissected the relationships between wider ecology and coevolutionary trajectory using 16 ecologically complex Daphnia magna-Pasteuria ramosa ponds seeded with an identical starting host (Daphnia) and parasite (Pasteuria) population. We show, using a time-shift experiment and outdoor population data, how multivariate biotic and abiotic ecological differences between ponds caused coevolutionary divergence. Wider ecology drove variation in host evolution of resistance, but not parasite infectivity; parasites subsequently coevolved in response to the changing complement of host genotypes, such that parasites adapted to historically resistant host genotypes. Parasitism was a stronger interaction for the parasite than for its host, likely because the host is the principal environment and selective force, whereas for hosts, parasite-mediated selection is one of many sources of selection. Our findings reveal the mechanisms through which wider ecology creates coevolutionary hotspots and coldspots in biologically realistic arenas of host-parasite interaction, and sheds light on how the ecological theatre can affect the (co)evolutionary play. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2020 |
| Provided To Others? | Yes |
| URL | http://datadryad.org/stash/dataset/doi:10.5061/dryad.qv9s4mwd6 |
| Title | Microsatellite marker data for Chernobyl Daphnia populations |
| Description | Populations experiencing varying levels of ionising radiation provide an excellent opportunity to study the fundamental drivers of evolution. Radiation can cause mutations, and thus supply genetic variation; it can also selectively remove individuals that are unable to cope with the physiological stresses associated with radiation exposure, or non-selectively cull swathes of the population, reducing genetic variation. Since the nuclear power plant explosion in 1986, the Chernobyl area has experienced a spatially heterogeneous exposure to varying levels of ionising radiation. We sampled Daphnia pulex (a freshwater crustacean) from lakes across the Chernobyl area, genotyped them at ten microsatellite loci, and also calculated the current radiation dose rates. We then investigated whether the pattern of genetic diversity was positively associated with radiation dose rates, consistent with radiation-mediated supply of de novo mutations, or negatively associated with radiation dose rates, as would be expected with strong radiation-mediated selection. We found that measures of genetic diversity, including expected heterozygosity and mean allelic richness (an unbiased indicator of diversity) were significantly higher in lakes that experienced the highest radiation dose rates. This suggests that mutation outweighs selection as the key evolutionary force in populations exposed to high radiation dose rates. We also found significant but weak population structure, indicative of low genetic drift, and clear evidence for isolation by distance between populations. This further suggests gene flow between nearby populations is eroding population structure, and that mutational input in high radiation lakes could, ultimately, supply genetic variation to lower radiation sites. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2022 |
| Provided To Others? | Yes |
| URL | http://datadryad.org/stash/dataset/doi:10.5061/dryad.0cfxpnw48 |
| Title | VBD models |
| Description | Using a pair of disease models (for mosquito- and tick-borne disease), we simulated how different types of change in host biodiversity led to either increased or decreased levels of disease in the system (measured as densities of infected vectord, proportion of infected hosts etc.) |
| Type Of Material | Computer model/algorithm |
| Provided To Others? | No |
| Impact | These models are novel in that they explicitly include vector biology in assessing how biodiversity change affects disease in natural systems. This is of profound importance when considering how changes in vector densities may affect the spread of vector-borne disease (e.g., Zika virus). |
| URL | http://dx.doi.org/10.5061/dryad.t24pq |
| Description | Radiation TREE collaboration |
| Organisation | University of Stirling |
| Country | United Kingdom |
| Sector | Academic/University |
| PI Contribution | I am co-supervisor of Ms Jessica Goodman, NERC PhD student (grant number NE/L000369/1). I am providing expertise on understanding how freshwater invertebrate populations have undergone evolutionary change as a result of both chronic and acute exposure to radiation. |
| Collaborator Contribution | Prof. David Copplestone (PI) has provided the PhD student researcher and radioecology expertise that matches with my evolutionary biology experience |
| Impact | None as yet. |
| Start Year | 2015 |
| Description | Voyage to Galapagos |
| Organisation | National Center for Science Education, USA |
| Country | United States |
| Sector | Charity/Non Profit |
| PI Contribution | I am a scientific advisor to the NCSE, which defends and promotes the teaching of evolution both within the US and internationally. We are developing an online educational resource that examines the impact of climate change on disease evolution and epidemiology, with the ultimate aim of looking at how climate change will impact on human health. The NCSE have been involved with the development of this NERC IRF proposal from the early stages, and the project's findings will be used as a basis for online student-led learning resources - essentially interactive games where the student (school, university or graduate level) navigates through the game to collect data, test hypothesis and understand the evolutionary and epidemiological processes that drive disease severity and spread. I am involved with ensuring the scientific accuracy of these games. |
| Collaborator Contribution | This collaboration has provided an impact outcome for my research. |
| Impact | This collaboration is multidisciplinary between educational and biological researchers. It will result in online student-led learning resources that teach concepts in evolution and epidemiology. |
| Start Year | 2014 |
| Description | BBC interview associated with paper "Sex as a strategy against rapidly evolving parasites" |
| 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 | Interview with Good Morning Scotland on BBC Radio Scotland. This interview brought the project's research to a wider audience, engaging the general public with primary research. The interview was followed with requests for involvement in newspaper articles and led to increased engagement over social media.I was also invited to give a seminar at the University of Zurich after this interview. |
| Year(s) Of Engagement Activity | 2016 |
| Description | Departmental seminar - Pirbright Institute |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | Regional |
| Primary Audience | Professional Practitioners |
| Results and Impact | I gave a seminar at the Pirbright Institute which sparked questions and lively discussion. |
| Year(s) Of Engagement Activity | 2016 |
| Description | Departmental seminar - University of Zurich |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Other audiences |
| Results and Impact | I gave an hour long talk to ~100-150 academics, postgrad and undergrad students. This led to discussion and lively debate. |
| Year(s) Of Engagement Activity | 2017 |
| Description | International Entomology conference (Florida) |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Other audiences |
| Results and Impact | Invited talk at Entomology 2016. |
| Year(s) Of Engagement Activity | 2016 |
| Description | Media associated with paper "Sex as a strategy against rapidly evolving parasites" |
| 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 | Media (as a channel to the public) |
| Results and Impact | We issued a press release for the Proceedings of the Royal Society manuscript "Sex as a strategy against rapidly evolving parasites". This attracted significant attention and resulted in articles in print media worldwide (including but not limited to: The Metro, The Daily Mail, The Independent, The Mirror, The Japan Times, El Pais; BBC website). This has sparked significant discussion over newspaper comments sections, as well as increased engagement in my research via email and social media. |
| Year(s) Of Engagement Activity | 2016 |
| Description | Pint of Science |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | Local |
| Primary Audience | Public/other audiences |
| Results and Impact | Pint of Science is a science festival that aims to communicate contemporary scientific developments to the public in an interesting, engaging and approachable way by bringing scientists to the pub and other accessible places. My talk was on "Why does sex exist?" |
| Year(s) Of Engagement Activity | 2018 |
| Description | Poster presentation - European Society for Evolutionary Biology |
| Form Of Engagement Activity | A talk or presentation |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Other audiences |
| Results and Impact | Conference poster presentation. ~1000 people viewed the poster and ~200 engaged with poster presentation, sparking questions and broader discussion. Audiences included research academics, postgraduates and undergraduates. |
| Year(s) Of Engagement Activity | 2017 |
| Description | Voyage to Galapagos |
| Form Of Engagement Activity | A formal working group, expert panel or dialogue |
| Part Of Official Scheme? | No |
| Geographic Reach | International |
| Primary Audience | Professional Practitioners |
| Results and Impact | The project's findings will be used as a basis for online student-led learning resources - essentially interactive games where the student (school, university or graduate level) navigates through the game to collect data, test hypothesis and understand the evolutionary and epidemiological processes that drive disease severity and spread. I am involved with ensuring the scientific accuracy of these games. None to date, the collaboration is ongoing and the software is still being designed. |
| Year(s) Of Engagement Activity | 2014 |