Rapid, parallel adaptation in the Anthropocene

Lead Research Organisation: Bangor University
Department Name: Sch of Natural Sciences

Abstract

As human activities have an increasingly detrimental effect on the natural environment it has become critically important to understand how habitats and species will cope with such rapid changes. The ability of a species to adapt is a crucial component of its resilience to climate change and this is reflected in recent attempts to include some component of adaptation in predictive models. However, we have a very poor understanding of the factors that might predict the evolvability of a species and so it is currently not possible to separate adaptive ability from plasticity, or broad niche breadth, based on the current environmental tolerances of a species. A first step in understanding whether evolution might be predictable in wild organisms is to understand the extent to which the adaptive process is repeatable and reproducible and what genomic signatures/features allow rapid adaptation to take place (making it identifiable).

To bridge this knowledge gap we need to study instances of contemporary parallel adaptation (<200 years), such as the rapid adaptation of Silene uniflora to heavy-metal contaminated soils at abandoned mines. This project will use state-of-the-art genetic/genomic analyses, quantitative genetics and experimental evolution studies. It will investigate the roles of standing genetic variation in the adaptive process, reveal the key signatures of rapid parallel evolution and investigate the potential for strong natural selection to drive reproductive isolation of populations at very small scales (i.e., a few meters). In so doing, it will uncover the genetic and genomic patterns that will help us to recognise and estimate the potential of plant species to adapt to rapid and extreme environmental change. As genome-scale sequencing becomes more accessible, it will be possible to analyse and assess genetic variation quickly and easily in any species. Hidden in this wealth of genomic data are the clues to whether species will adapt or perish; the proposed project will help researchers to decode those clues.

Planned Impact

Improvements to the public understanding and awareness of science: Silene uniflora (sea campion) is a common and charismatic feature of coastal habitats in the UK and Ireland. This rapid "evolution on our doorstep" provides a link between the objects people use daily (e.g. zinc galvanised products, copper wiring) and evolutionary processes and conservation. As such, S. uniflora is an excellent species to capture the attention of students and the public, promoting understanding of evolutionary genetics, speciation, conservation, human impacts on plant diversity and the ingenuity of plant responses to human disturbance. These benefits can be realised in the short and medium term through public interaction at events (e.g., the annual Science Festival events at RBG Kew and Pint of Science Festival) and by producing interpretation materials for the numerous SSSIs where the species occurs. Encouraging interest in plants and evolutionary biology in school children can be achieved via school visits organised with the public learning and engagement department at RBG Kew.

Training skilled people: The research will provide training in scientific skills that are transferable to professions outside academia. PDRA - the communication, bioinformatics/data processing, statistical and laboratory skills developed by the PDRA are widely transferable to biological science disciplines, as well as in non-scientific fields in industry. Technician - the experimental techniques (e.g., plant propagation), forward planning/time management and laboratory skills gained by the technician are transferrable to many areas of plant science and industry. Summer internships - development of skills in communication and interpretation will be invaluable to undergraduates/postgraduates interested in science communication, journalism and editing.

Conservation of biodiversity, management and improvement of contaminated sites: Heavily contaminated mine sites in the UK support unique ecosystems and metallophtye communities are of conservation interest and protected as Calaminarian grasslands under Annex I of the EU Habitats Directive. However, contaminated soils are also a source of pollution that can have detrimental effects on other natural systems and agricultural land (Navarro et al., J. Geochem. Explor. 96, 183-193, 2008). These phytotoxic metals also adversely affect soil microorganisms and are the most common heavy metal contaminants of agricultural land via atmospheric deposition in the UK (Defra research project SP0547, 2005). Phytostabilisation of polluted soils may be a fruitful method of ring-fencing and improving contaminated land. S. uniflora forms spreading vegetation mats on contaminated sites. Such pioneer, tolerant plants provide a vegetative cover that minimises leaching and movement of contaminated dust and soil, and can eventually lay down top soils which can act as a barrier, sealing off the polluted substrate. Understanding the genes underlying heavy-metal adaptation will allow identification of suitable plants for remediation efforts.

This project and future studies will feed into Defra's strategic priority of improving the natural environment and its strategic evidence priorities in sustainable management of natural resources and greater resilience in the natural environment. The outcomes will contribute to the evidence strategies of Natural England, Natural Resources Wales and the Joint Nature Conservation Committee, allowing conservation decisions to be based on sound scientific evidence. In the longer term, this research will make it possible to assess the usefulness of these plants for phytostabilisation of polluted soils. Phytostabilisation research would be valuable to statutory agencies in the UK and Ireland. It will also benefit industries which produce heavy-metal contaminants by providing potential methods to minimise the impact of their activities on natural systems.

Publications

10 25 50
 
Description 1. Rapid adaptation to a man made polluted environments has occurred repeatedly in fewer than 250 generations. In response to zinc and copper contamination, multiple populations of S. uniflora have evolved independently of each other. Although there is extensive migration between coastal/ancestral populations, the mine populations did not have a single origin that spread around to different mines. Nor has adaptive genetic material been transferred between the mines. Zinc and copper tolerance are not governed by the same mechanisms, with some populations displaying tolerance to both contaminants and others tolerant to only one, However, both tolerances have evolved rapidly in parallel in different regions of the UK and over small distances. This represents one of the only systems where parallel adaptation has been conclusively demonstrated within 100s of generations.

2. Surprisingly, rapid parallel adaptation has a complex genetic basis. The expectation was that we would find a small number of large effect genetic loci that drives parallel adaptation. Despite finding that there are some large effect genomic regions (via quantitative trait mapping), we discovered that very few mutations are shared across the replicated instances of metal tolerance evolution. Rather, parallelism between sites is manifested at the level of genes and gene functions, with alleles drawn from standing variation. In other words, the same adaptive outcome can be achieved by selecting different genetic variants in different sites, but the same genes and pathways will be adjusted to allow colonisation and survival. This fundamentally changes the way in which we understand the nature of genetic variation required for rapid adaptation to take place. Instead of strong selection driving large effect alleles to fixation, there are multiple pathways to successful rapid parallel adaptation. Therefore, this phenomenon may be much more common than expected, but the task of predicting evolutionary outcomes from genetic data is more complicated than hoped.

3. Ancestral plasticity and genetic assimilation contribute to rapid adaptation. Our experiments show that plasticity in the coastal population's response to zinc is dominated by a widespread stress response. However, we found evidence that ancestral plasticity facilitates adaptation for a substantial proportion of genes that are involved in adaptation in the mine populations, by moving gene expression towards the optimum level in the new environment. One third of constitutive differences between ecotypes are the result of genetic assimilation of ancestral plasticity. These results show, controversially, that ancestral plasticity plays a much larger role in rapid adaptation than expected.

4. Phenotypic plasticity can facilitate parallel adaptation by triggering the recruitment of the same genes in independent instances of adaptation. However, despite a high degree of convergence in gene expression levels between independently adapted lineages, genes with ancestral plasticity are as likely to have similar expression levels in adapted populations as genes without. In other words, plasticity does not drive parallelism in the level of expression of those genes, with expression levels more likely to reflect the concentrations and characteristics of the local sites.

Overall, we discovered frequent and rapid, parallel adaptation to human contaminated mine sites. Parallel adaptation is characterised by a complex genetic basis that relies on standing variation and ancestral plasticity, but does not always use he same genetic variants.
Exploitation Route These results have significant implications for understanding and predicting how wild organisms will respond to environmental change. It shows that rapid parallel adaptation can and does happen over short timescales relevant to human induced change. However, the complex genetic basis of adaptation may make the adaptive process harder to predict. This can be included in future models to understand evolutionary responses and taken into consideration when estimating the impact of environmental change on natural systems. This includes by researchers in the academic sector, as well as conservation and environmental practitioners.
Sectors Agriculture, Food and Drink,Environment,Manufacturing, including Industrial Biotechology

 
Description The COVID-19 pandemic limited the capacity of the research to produce impact in a number of ways (e.g. cancellation of engagement activities, restrictions on site visits etc). However, impact has been achieved through public engagement events targeted at school age children and at a much broader audience including industry and policy makers increasing awareness of the capacity of organisms to adapt rapidly to the environment, while leveraging the results from the project to demonstrate the challenges that are posed in predicting how environmental change will affect adaptive processes. In an academic context, the research has broken new ground on the complexity of the genetic basis of parallel adaptation and the role of plasticity in parallel adaptation, which is leading to the building of collaborative networks focused on studying and understanding these processes across a range of organisms. The resources are stimulating growth and have secured funding in new research areas on adaptation as well as providing a wider resource producing collaboration and advancing research in plant genomics, sex chromosome evolution, pangenome analyses and conservation genetics. Impact in industry has not been developed yet. However, we are conducting experiments based on those in the research to test the capacity of the species to accumulate lithium at a rate that might make the plants a viable lithium extraction method, which provides a promising route for future economic impact.
First Year Of Impact 2019
Impact Types Cultural,Societal

 
Description (PANDORA) - Paradigm for Novel Dynamic Oceanic Resource Assessments
Amount € 5,598,389 (EUR)
Funding ID 773713 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 04/2018 
End 04/2022
 
Description Adapting to extreme environments: hybridisation and the evolution of contemporary heavy metal tolerance
Amount £75,000 (GBP)
Funding ID 2431120 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2020 
End 03/2024
 
Description Drought vulnerability of the date palm and its wild relatives
Amount £75,000 (GBP)
Funding ID 2595827 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2021 
End 03/2025
 
Description Wallacea region - understanding biodiversity and evolutionary responses to environmental change
Amount £693,190 (GBP)
Funding ID NE/S006893/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 11/2018 
End 11/2021
 
Title Linkage maps for Silene uniflora 
Description Genetic maps for three families of Silene uniflora 
Type Of Material Improvements to research infrastructure 
Year Produced 2021 
Provided To Others? No  
Impact Allows research on the recombination landscape and structural variation in Silene uniflora, other Silene species and Caryophyllaceae more broadly. Curretnly used in research on the evolution of heavy metal tolerance (via analysis of quantitative trait loci), rapid adaptation and the evolution of SIlene sex chromosomes and for understanding genomic architecture in other Silene species (by collaborators). The linkage maps will be publicly available on publication and are currently available on request 
 
Title Reference genome for Silene uniflora 
Description Reference genome of Silene uniflora from an inbred line generated in this project (N50 27MB, L50 12). 
Type Of Material Improvements to research infrastructure 
Year Produced 2019 
Provided To Others? No  
Impact Design of sequencing primers for student projects. Design of SNP assay panel for Silene uniflora (25k SNPs). Used for analysis of the genetic basis of metal tolerance, rapid adaptation and sex chromosome evolution (within the team) and for understanding genomic architecture in other Silene species (by collaborators). The genome assembly will be publicly available on publication and is currently available on request 
 
Title Reference transcriptome for Silene uniflora 
Description The first reference transcriptome sequence for Silene uniflora 
Type Of Material Improvements to research infrastructure 
Year Produced 2021 
Provided To Others? Yes  
Impact Allows research on the genetic basis and role of plasticity in Silene uniflora, as well as being integral to the annotation of the reference genome. As a result the transcriptome is facilitating research in Silene species and Caryophyllaceae more broadly. Currently used in research on the role of phenotypic plasticity during rapid parallel evolution of heavy metal tolerance. 
 
Title Heavy metal tolerance records for Silene uniflora 
Description Zinc tolerance measurements for 51 Silene uniflora populations. To be deposited with EIDC. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact Used to determine frequency of the rapid evolution of metal tolerance. Used in undergraduate research projects to design sampling stratergies 
 
Title Plant collections of Silene uniflora 
Description Preserved tissue samples were collected from all populations in the study. Living plants were also grown from seeds or cuttings and are maintained in a living collection at Bangor University. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? No  
Impact The tissue collections were used to generate genomic resources for the project. Living samples were used for crosses and to conduct metal tolerance experiments. the specimens continue to be used for PhD student (eg, adaptive introgression, genetic basis of salt tolerance) and undergraduate projects (e.g. parallel evolution of reproductive isolation), as well as providing a resource for work outlined in new collaborations, eg (pangenome construction). 
 
Title Reduced representation sequencing for F2 crosses 
Description Reduced representation sequencing of 549 Silene uniflora individuals from three experimental crosses. Data to be made publicly available upon publication. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact These data have been used to generate genetic maps for the species and are being used to determine the genetic basis of zinc tolerance, which has been located to a single large effect locus. Data will be made publicly available upon publication. 
 
Title Reduced representation sequencing of copper transects 
Description Reduced representation sequencing of 425 Silene uniflora individuals from three transects across gradients of copper contamination in Cornwall. Data will be made publicly available upon publication. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact Currently used to investigate the genetic basis of copper tolerance during rapid adaptation. 
 
Title Silene uniflora gene expression 
Description RNA sequencing of 12 Silene uniflora individuals grown under two experimental conditions. Data to be made publicly available upon publication. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact This data has been used to investigate the role of genetic assimilation and phenotpyic plasticity in rapid parallel evolution. The research is under review and available as a preprint. 
 
Title Silene uniflora genome resequencing 
Description Whole genome resequencing for 604 individuals of Silene uniflora from 62 populations. To be made publicly available on publication. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact Used to determine the frequency and genetic basis of rapid evolution of metal tolerance. Used in undergraduate research projects to design sampling strategies and in a PhD project to investigate adaptive introgression 
 
Title Site records for Silene uniflora 
Description Site records for populations studied. To be deposited with EIDC. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact Used to determine frequency of the rapid evolution of metal tolerance. Used in undergraduate research projects to design sampling stratergies 
 
Description ADAPT Network - AF 
Organisation Norwegian University of Science and Technology (NTNU)
Country Norway 
Sector Academic/University 
PI Contribution Contributed to ADAPT network organisation, networking events and publications arsing form the network
Collaborator Contribution Contributed to ADAPT network organisation, networking events and publications arsing form the network
Impact Manuscript in evolution letters
Start Year 2018
 
Description Adaptive introgression - MF 
Organisation Royal Botanic Gardens, Kew
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Developed new project and secured funding for PhD student. Provides genomic resources from current project to support analyses.
Collaborator Contribution Expertise in botanical area and genetics of UK species, links to collaborative network. Host research visit/placement for student
Impact Secured PhD funding. Collaborated on published manuscript in Molecular Biology and Evolution
Start Year 2018
 
Description Caryophyllaceae genome evolution - DS 
Organisation Colorado State University
Country United States 
Sector Academic/University 
PI Contribution Our team have contributed genomic resources (genome sequence, linkage maps, genome annotations) to enhance research on the evolution of genomic diversity in Caryophyllaceae
Collaborator Contribution The partners have provide genomic resources for other Caryophyllaceae species to enhance research on the evolution of genomic diversity in Caryophyllaceae
Impact Collaboration is in its early stages, manuscripts facilitated by this collaboration are pending.
Start Year 2021
 
Description Genomics-LTD 
Organisation University of Sheffield
Country United Kingdom 
Sector Academic/University 
PI Contribution We created an inbred line of Silene uniflora, extracted DNA and quality controlled samples needed for long read library preparation and sequencing.
Collaborator Contribution Our collaborator (LTD, University of Sheffield) produced 7kb pacbio sequencing libraries from low integrity samples and contributed code for genome assembly.
Impact SU_WGS
Start Year 2018
 
Description Pangenomics of metal tolerant species - LY 
Organisation University of Nottingham
Country United Kingdom 
Sector Academic/University 
PI Contribution This collaboration uses the genomic resources, collections and extracted DNA generated during the project to expand the pan-genome for the study species. The collaboration focuses on producing new long read assemblies generated at UoN to advance our understanding of structural rearrangement in rapid adaptation. Our reasearch team will also contribute to data anlysis
Collaborator Contribution The partner (LY) has contributed the genomic library preparations and Promethion sequencing for the collaboration, as well as committing staff time to the initial data analysis of the long reads and pangenome construction.
Impact The new genome sequencing generated. We are awaiting the outcome of an ENVISION DTP application on mine adaptation.
Start Year 2021
 
Description Serpentine adaptation in Silene uniflora -TQ 
Organisation University of Vigo
Country Spain 
Sector Academic/University 
PI Contribution Collections of samples and genomic data for Silene uniflora in the UK, including from serpentine sites. Data analysis.
Collaborator Contribution Collection of Silene uniflora specimens form Spanish coastal and serpentine sites.
Impact research ongoing, genetic dataset and tolerance records expanded based on new samples
Start Year 2020
 
Description Sex chromosome evolution in silene - PT 
Organisation University of Lille
Country France 
Sector Academic/University 
PI Contribution Generation of genomic resources for Silene uniflora and analysis of sex chromosome evolution.
Collaborator Contribution development of ideas for publication and transcriptomic resources for Silene species with sex chromosomes.
Impact Manuscript in preparation
Start Year 2021
 
Description Festival of Discovery 
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 The Festival of Discovery (Anglesey) was a three day festival with an area devoted to Bangor University Science and Technology. The science area was visited by 4500 members of the general public and activities were directed towards 5-16 year olds. The project team (ASTP and DW) organised an interactive display with games and activities to promote understanding of natural selection, evolution and adaptation, with a particular focus on parallel adaptation in S. uniflora and other examples from the UK. Feedback from visitors a was overwhelmingly positive.
Year(s) Of Engagement Activity 2019
URL https://www.bangor.ac.uk/bangorsciencefestival/
 
Description Genepark presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact The Genetic and Genomics for the 3rd Generation (3G) conference was an event at the Wales Gene Park as part of the Wales Festival of Innovation. The conference consisted of a series of talks from researchers detailing their genetics/genomics research and how it impacts our everyday lives, aimed at the general public. It was primarily aimed at members of the public aged over 50, with members of third-sector organisations such as the WI and the University of the 3rd Age attending. It was part of the Wales Festival of Innovation aiming to highlight cutting edge research and development taking place in Wales. A 25 minute presentation was given outlining the scope of the research, with a particular emphasis on how genetic/genomic techniques can be used to answer questions of interest to evolutionary biologists. Approximately 50 people were in attendance, and feedback from the conference organisers indicated a positive response to the talk.
Year(s) Of Engagement Activity 2019
 
Description State of the world's plants and fungi symposium 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact An invited presentation for the State of the world's plants and Fungi symposium at Royal Botanic Gardens Kew. Alex Papadopulos contributed a presentation on day 2. The event was attended online by 3000 participants and has subsequently received 1700 views on youtube. The presentation generated discussion on the adaptation to environmental change and was contacted for further information by the Food and Agriculture Organization of the United Nations.
Year(s) Of Engagement Activity 2020
URL https://www.youtube.com/watch?v=QYiCgmnysCU
 
Description bsx3139-minisymposium 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact Daniel wood presented the research and current findings at a mini symposium of postdoctoral research directed at 3rd year undergraduates as part of a molecular ecology and evolution module organised by Alex Papadopulos. The aim was to promote research into evolutionary biology and adaptation in plants among undergraduates and inspire the next generation of scientist.
Year(s) Of Engagement Activity 2018,2019,2020
 
Description website 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Website promoting research and activities conducted in the research group, primarily focused on the activities in this research grant. The purpose is to raise awareness of the effects and research into extreme environmental changes specifically regarding adaptation. The website receives ~10 visitors per day with 15,000 visitors in the last 12 months (2018/19).
Year(s) Of Engagement Activity 2018,2019
URL http://labadopulos.co.uk