LIMITS TO ADAPTATION: CAUSES, AND CONSEQUENCES FOR ECOLOGY AND ECOSYSTEM FUNCTION

Lead Research Organisation: University of Liverpool
Department Name: Institute of Integrative Biology

Abstract

Species are increasingly faced with the challenge of coping with a changing environment caused by human disturbance or climate change. Whether they are able to cope or not is critical for biodiversity and the benefits that we get from ecosystems. The ability of species to evolve and adapt to new environmental conditions is a key factor that we need to understand if we are to predict how species will cope with a changing environment or to help mitigate the impacts of climate change. It is particularly important to understand how rapidly species can adapt, what the limits are to evolution, and how evolution of one species will affect the rest of the ecosystem with which it interacts.

In this project, we will investigate these questions through a series of large scale experiments using a small crustacean called Daphnia, which has a major impact on water quality and the health of freshwater ecosystems. Our approach has several unique strengths. First, Daphnia can reproduce clonally, which means that we can manipulate the genetic diversity of populations to examine its effects on the rate and limits of adaptation. Second, we will use a system of large outdoor heated tanks - the largest such facility in Europe - to examine the response of Daphnia, and its associated ecosystem, to heat-waves, which is a key environmental challenge faced by species. Third, we will exploit the latest DNA sequencing technologies - available at a major genomics centre at Liverpool - to examine the genetic mechanisms underlying adaptation to climate change. Finally, our study is supported by recent, exciting findings from our laboratory where we have demonstrated the potential importance of two processes - plasticity and epigenetics - for adaptation. Plasticity allows individuals to change their pattern of development, growth and/or reproduction in response to the environment, and epigenetics allows these changes to be transmitted to their offspring by modifying the action of genes. These processes are central to questions about what limits the ability to adapt to environmental change, since they could allow the animals to adapt far more rapidly than they would by conventional evolution alone, in which only frequencies of genes change over time. As such, these processes may also help protect the animal populations from going extinct following an environmental change, so allowing time for the species to evolve over a longer period.

The research will: i) quantify how two major influences on animals (food and temperature differences) affect many different and crucial aspects of the lives of Daphnia (phenotypic plasticity); ii) use the knowledge of this plasticity together with whether the Daphnia are adapted to local or different environments, to undertand how plasticity, genetic diversity and epigenetics determine the potential of populations to evolve; iii) understand how limitations in the potential of populations to evolve will alter the fate of other species in the community and the functioning of the whole ecosystem (e.g. by regulating water quality and blooms of harmful algae).

This research will, therefore, fundamentally advance our understanding of how three different influences (genetic diversity, plasticity and epigenetics) contribute and combine to allow populations to adapt to environmental change, and how this can affect other species and ultimately the services (clean water, food, fibre, amenity) that freshwater ecosystems and their biodiversity provide. Our findings will be disseminated to the academic community, to policy-makers, to schools and to the general public.

Planned Impact

Policy makers:
A greater understanding of the mechanisms that either hasten extinction or underpin rapid evolutionary responses to anthropogenic stressors, and the effect that this then has on population, community and ecosystem level processes will help environment and health legislators to deliver informed conservation, medical and sustainable harvesting strategies that will mitigate or avoid anthropogenic effects, and/or protect the evolutionary processes that determine future patterns of biodiversity.

Training of scientists:
The project will train researchers in state-of-the-art 'omic techniques that are transferable to other fields such as health and medicine, stem cell technology, disease biology, agriculture, conservation, and environmental sciences. The conceptually broad and integrative nature of this project - investigating links along pathways between molecular biology and ecosystem function - will not only train researchers in several specialist areas of life and environmental sciences, but crucially also in working in multidisciplinary teams to advance a more thorough and comprehensive understanding of complex environmental challenges.

Commercial/private sector:
Understanding individual, population, community and ecosystem level responses to human-induced evolutionary change can help us to mitigate these effects in natural environments. But also, a mechanistic understanding of rapid evolutionary responses might also be used to improve responses to artificial selection used in agriculture and food industries.

Wider public:
Concepts such as contemporary evolution, phenotypic plasticity, non-genetic inheritance and epigenetics are complex topics that are poorly understood by the general public. Yet they are increasingly an everyday part of our lives, impacting on society through antibiotic and pesticide resistance, the over-harvesting of natural resources, and their implication in diseases including aging, cancer, schizophrenia and lifestyle diseases such as heart disease, diabetes, and obesity. Our work will improve the public understanding of science by introducing these topics into the public domain. Second, the wider public will also benefit from our work because incorporating rapid evolution into the management of shallow freshwaters will help to protect them and the ecosystem services that they provide, including the provision of freshwater, power-generation, regulation of waste and nutrients, retention of soil and transport and recreation.
 
Title Article for Gentian magazine 
Description Plaistow co-wrote an article for The Gentian magazine (a magazine for the members of Ness Botanic Gardens) explaining the environmentally friendly technology used to build a new mesocosm laboratory next to our ponds. The Adhesive-Free Timber Buildings (AFTB) project was led by investigator Dr Zhongwei Guan, and supported by a four-year, €4.8M European Regional Development Agency grant 
Type Of Art Creative Writing 
Year Produced 2020 
Impact Article yet to be published 
 
Title Things are getting hot in the ponds at Ness 
Description A short article reporting the findings of our study for 'Nature matters', a Warwickshire naturalist publication. 
Type Of Art Creative Writing 
Year Produced 2021 
Impact The article was requested following individuals seeing an outreach display at our research site. It is essentially to provide an update on our research findings that a lay person would be able to follow relating to what limits the evolutionary potential of shallow freshwaters. 
 
Description We have demonstrated that multivariate plastic responses explained more than 30% of the total phenotypic variation in different temperature and food environments. Genetic variation in plastic responses is detectable in most environment combinations but the nature of the variation was context-dependent resulting in environment-specific differences in evolvability in populations. We found little evidence that genetic variation in traits linked to food and temperature are aligned with the plastic responses to food and temperature suggesting that it may be harder for populations to further evolve in response to heat-related stressors. This was confirmed by our mesocosm studies which demonstrated that heatwaves do not induce rapid evolutionary change and broader community and ecosystem effects in community embedded Daphnia magna populations. Instead, heatwaves induce a transient effect on both Daphnia magna phenotypes and the community dynamics of shallow freshwaters which reverses after a few months. These effects are the result of plasticity rather than rapid reversible shifts in clone frequencies. Our findings contrast with previous studies that have concluded that there is the potential for temperature induced rapid adaptation in Daphnia populations. However, these studies have not used realistic thermal manipulations, and often use experiments that mimic populations experiencing strong selection for rapid population growth which selects for clones with smaller body sizes. This may look like rapid thermal adaptation because thermal tolerance is genetically correlated with body size. Our epigenetic work has demonstrated that temperature does induce changes in patterns of DNA methylation but these patterns are DNA methylation are clone-specific, suggesting that genetic and non-genetic inheritance is not independent in this species.
Exploitation Route Our findings will hopefully provide one of the most thorough examples of how a population that is embedded in a natural community in a semi-natural environment responds to an increased frequency of heatwaves.
Sectors Education

Environment

 
Description Our findings are having an impact on the public understanding of science. Our mesocosm facility is situated in a botanic gardens that receives thousands of visitors a year. We have created a digital poster that uses QR codes to link the public to video resources that explain the project, it's significance and what the outcomes are and what they mean.
First Year Of Impact 2021
Impact Types Societal

 
Description A non-destructive dynamic assay of egg development in Daphnia
Amount £15,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 04/2023 
End 06/2023
 
Description Evolutionary resistance: Does adaptation stabilise plant community structure and function under climate change?
Amount £647,858 (GBP)
Funding ID NE/R011451/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 07/2018 
End 01/2022
 
Description Internal funding
Amount £100,000 (GBP)
Organisation University of Liverpool 
Sector Academic/University
Country United Kingdom
Start 12/2016 
 
Description NERC Doctoral Training Program
Amount £60,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2020 
End 09/2024
 
Description UKRI Covid 19 allocation fund
Amount £37,576 (GBP)
Organisation United Kingdom Research and Innovation 
Sector Public
Country United Kingdom
Start 08/2020 
End 09/2020
 
Title Semi-automated Daphnia population counts 
Description We have developed a semi-automated image analysis technique for studying Daphnia population dynamics 
Type Of Material Biological samples 
Provided To Others? No  
Impact Allows the study of eco-evolutionary feedback loops 
 
Title University of Liverpool experimental freshwater mesocosms 
Description We have built 50 x 3000 litre freshwater 'smart' mesocosms that are fully temperature controllable and incorporate telemetric collection of data. The facility allows us to program heatwaves into shallow freshwaters and study the environmental consequences. 
Type Of Material Improvements to research infrastructure 
Year Produced 2017 
Provided To Others? No  
Impact The facility will allow the controlled and replicated study of the effects of warming on semi-natural shallow freshwater communities. 
URL https://smartponds.liverpool.ac.uk/Ness%20Summary/index.html
 
Title ENA Database (Project number: PRJEB50055) - Whole genome bisulfide sequencing of Daphnia magna clones 
Description Different clones of Daphnia magna, a freshwater crustacean, were assayed by whole genome bisulfide sequencing at either 21C or 28C either under a continuous temperature regime or under a switched regime. The aim was to determine whether genotype or environmental temperature had a greater effect of the distribution of differentially methylated CpG sites. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
Impact None as yet 
URL https://www.ebi.ac.uk/ena/browser/view/PRJEB50055?show=reads
 
Title Hourly temperature, environmental parameter and Daphnia magna phenotypic and genetic change in mesocosms with manipulated experimental parameters, 2017-2019 
Description This dataset contains information about hourly temperature variation, phenotypic and genetic change, and change in environmental parameters in a two-year mesocosm study designed to tease apart the impact that phenotypic plasticity and genetic diversity have on rate of adaptation to experimental heatwaves. All data were collected between 2017 and 2019. Thermal data was collected continuously using data loggers. The frequency of natural heatwaves was manipulated using a programmable aquatic mesocosm facility using data collected from real heatwaves from 2006. Phenotypic evolution was tracked using intermittent common garden life-history studies while changes in clone frequency were determined using microsatellite markers to track changes in clone frequency in manipulated populations over two years. Experimental data on zooplankton community dynamics were monitored using intermittent depth integrated sampling of communities in each mesocosm over two years. The work was supported by the Natural Environment Research Council (Grant NE/N016017/1). 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
Impact Not yet 
URL https://catalogue.ceh.ac.uk/id/2ae5e8d3-be36-4517-b80c-c6b91792b769
 
Title Pollution induces epigenetic effects that are stably transmitted across multiple generations 
Description It has been hypothesised that the effects of pollutants on phenotypes can be passed to subsequent generations through epigenetic inheritance, affecting populations long after the removal of a pollutant. But there is still little evidence that pollutants can induce persistent epigenetic effects in animals. Here we show that low doses of commonly used pollutants induce genome-wide differences in cytosine methylation in the freshwater crustacean Daphnia pulex. Uniclonal populations were either continually exposed to pollutants or switched to clean water, and methylation was compared to control populations that did not experience pollutant exposure. While some direct changes to methylation were only present in the continually exposed populations, others were present in both the continually exposed and switched to clean water treatments, suggesting that these modifications had persisted for seven months (> 15 generations). We also identified modifications which were only present in the populations that had switched to clean water, indicating a long-term legacy of pollutant exposure distinct from the persistent effects. Pollutant-induced differential methylation tended to occur at sites that were highly methylated in controls. Modifications that were observed in both continually and switched treatments were highly methylated in controls and showed reduced methylation in the treatments. On the other hand, modifications found just in the switched treatment tended to have lower levels of methylation in the controls and showed increase methylation in the switched treatment. In a second experiment we confirmed that sub-lethal doses of the same pollutants generate effects on life-histories for at least three generations following the removal of the pollutant. Our results demonstrate that even low doses of pollutants can induce transgenerational epigenetic effects that are stably transmitted over many generations. Persistent effects are likely to influence phenotypic development, which could contribute to the rapid adaptation, or extinction, of populations confronted by anthropogenic stressors. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
Impact Not yet 
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.h9w0vt4k9
 
Title Population level plasticity assays (temp x food) 
Description A comparison of multivariate plasticity generated by temperature and food for 75 clones from a single population and 30 clones from other thermal niches. 
Type Of Material Database/Collection of data 
Provided To Others? No  
Impact In progress 
 
Description Prof. Roy Goodacre 
Organisation University of Liverpool
Country United Kingdom 
Sector Academic/University 
PI Contribution We are developing a technique for using RAMAN spectroscopy as a tool to understand the transmission of maternal environment effects (pollutants/micro plastics) to subsequent generations. My lab is delivering all aspects of Daphnia biology and the inspiration for the project and links to eco-tox labs.
Collaborator Contribution Prof. Goodacre's lab are providing access to RAMAN technology and developing a techniques for screening single eggs.
Impact NEOF ECR grant application
Start Year 2019
 
Description Tom van Dooren 
Organisation École Normale Supérieure, Paris
Country France 
Sector Academic/University 
PI Contribution We are working on how Tom can use the data collected from this grant tp parameterise models of evolutionary lag.
Collaborator Contribution We are working on how Tom can use the data collected from this grant tp parameterise models of evolutionary lag.
Impact Harney E.H., Van Dooren, T.J.M., Paterson, S & Plaistow, S.J. (2013) How to measure maturation: a comparison of probabilistic methods used to test for genotypic variation and plasticity in the decision to mature. Evolution, 67(2), pp. 525-538. Van Dooren, T.J.M., Hoyle, R.B., & Plaistow, S.J. (2016) Maternal Effects. In: Kliman, R.M. (ed.), The Encyclopedia of Evolutionary Biology. vol. 2, pp. 446-452. Oxford: Academic Press.
Start Year 2016
 
Description A-Level conference, UTC Liverpool 
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 Dr Ian Wilson judged final year research presentations for a science-career focussed college we work with and talked about our research.
Year(s) Of Engagement Activity 2019
 
Description BES Thematic topic 2016 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact I organised a thematic session on rapid evolution and invited speakers from various European institutions to contribute.
Year(s) Of Engagement Activity 2016
 
Description BES special interest group meeting on climate change 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Dr Franzi Brunner presented aspects of our findings on consequences of heatwaves to a BES special interest group in York on extreme climatic events.
Year(s) Of Engagement Activity 2019
 
Description Birmingham seminar 2017 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact Research seminar
Year(s) Of Engagement Activity 2017
 
Description Family Science fair (British Science week) 
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 The activity involved table-top pond-dipping and microscope work for kids and active discussion about research goals for adults. The day was successful and received lots of good feedback.
Year(s) Of Engagement Activity 2018,2019,2020
URL https://www.liverpool.ac.uk/ness-gardens/whats-on/events-ness/familysciencefair.html
 
Description Gardeners question time event at Ness Gardens 
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 We led adult pond-dipping sessions and gave multiple talks about our research project to members of the public. This resulted in numerous questions from the public about climate change and organisms response to it and some feedback on twitter etc.
Year(s) Of Engagement Activity 2017
 
Description Mechanisms underpinning intergenerational change 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Plaistow presented results from the project at a meeting in Cambridge on mechanisms underpinning intergenerational change 24-26/09/19. The meeting was designed to forge overall between evolutionary biologists interested in transgenerational effects and researchers working primarily on foetal programming.
Year(s) Of Engagement Activity 2019
URL https://coursesandconferences.wellcomegenomecampus.org/our-events/mechanisms-and-evolution-of-interg...
 
Description Non-Genetic Inheritance workshop (Moulis, France) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact 20 + experts in non-genetic inheritance will meet to give talks and discuss the evolutionary significance of NGI
Year(s) Of Engagement Activity 2017
 
Description Outreach event (Alderhey hospital) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Dr Ian Wilson post-doc) prepared a poster and activities for 50-100 children/members of the public to learn about how we use waterfleas to understand rapid adaptation to heatwaves
Year(s) Of Engagement Activity 2019
 
Description Public engagement with research event 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Our research team will take part in an event designed to interface research conducted at the university with the public.
Year(s) Of Engagement Activity 2017
 
Description Research talk at QMUL 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Other audiences
Results and Impact Plaistow presented a research talk on recent findings from our group and the progress to date on this project
Year(s) Of Engagement Activity 2018
 
Description Royal Society partnership grant film 
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 Schools
Results and Impact Our Royal Society funded partnership grant was featured in a Royal Society video designed to promote the partnership scheme.
Year(s) Of Engagement Activity 2016
URL https://youtu.be/I5ljysxh6gE
 
Description School visit x 3 (Liverpool, UTC) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk introducing pupils to non-genetic inheritance and its ecological, evolutionary and health consequences
Year(s) Of Engagement Activity 2015,2016
 
Description Visit to IGB (Limnology Institute), Berlin 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Plaistow visited and gave talks about our work at the Lake Lab (Lake mesocosms), IGB, and Frei Universitat. The aim was to integrate our mesocosm facilities with a global mesocosm network run by Prof. Jens Nejstgaard (Lake Lab) and develop future collaboration.
Year(s) Of Engagement Activity 2019