The Great Tit HapMap Project

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

Abstract

Most people interested in science are aware that the last decade has witnessed dramatic advances in genomics tools and techniques.
Excitingly, these new technologies are not limited to humans or classical model organisms like fruitflies and yeasts, but can now be applied to organisms which have long interested ecologists but which, until now, lacked genetics tools. We have taken advantage of the opportunities afforded by so-called next generation sequencing to develop genomics resources for the great tit.

Great tits (Parus major) are one of the most widely studied invertebrates because they are common and readily breed in artifical nest boxes. As a result a number of long term studies of great tit populations have been conducted across Europe, some of which have been ongoing for more than 50 years and include data on tens of thousands of individual birds.
These long-term datasets are rich resources for studying important ecological questions such as: How organisms adapt to climate change, How organisms allocate resources to breeding and other activities, How species evolve in the face of natural selection.

Using funds won from the European Research Council (ERC) and the Netherlands government, we have begun to map genes responsible for variation in life history and morphological traits in two of the most intensively studied populations - at Wytham Woods in the UK and de Hoge Veluwe in The Netherlands. By working as a UK-Dutch collaboration we have pooled genomics resources and developed a tool called a SNP chip which allows us to type more than 9000 genetic markers in each of our study populations. We have now typed more than 2000 Dutch birds and 2700 UK birds with this chip. In this proposal, we request funds to type a further 16 great tit populations (50 birds per population). Why do we want to do this? The main reason is that by typing the same genetic markers in lots of different populations we can characterise genetic variation across the entire species range in order to learn more about the species evolutionary history. Projects of this nature are sometimes called HapMap Projects because they involve the mapping of markers linked along a chromosome (HAPlotypes). The best known HapMap project has been conducted in humans and has led to great insight into how our species colonised the world after migrating from Africa, how different populations are related to each other, and how genes have enabled us to adapt to e.g. different environmental conditions, novel challenges such as emerging diseases, changes in diet etc. By carrying out a Great Tit HapMap Project we can address similar questions in this widely studied ecological model organism. This also means we can extend the findings from the Wytham and de Hoge Veluwe populations to ask fundamental questions about evolutionary genetics. For example: Do the same genes explain adaptation in different populations? Do beneficial genes that arise in one population rapidly spread to other populations? Do the genes that explain variation within a population also explain differences between populations? Does migration between populations play a major role in maintaining genetic diversity? Does this gene flow help or hinder local adaptation?

There is perhaps no other vertebrate for which multiple long-term ecological datasets and such extensive genomics resources are available. Therefore, the great tit is an ideal organism in which to perform the first 'natural population' HapMap Project.

Planned Impact

Our project addresses fundamental questions in evolutionary genetics; as such it is largely blue-skies research and will advance understanding of the genetic architecture of quantitative genetic variation. Apart from standard activities (attending conferences, publishing our research, and presenting scientific seminars) we intend to engage in the following impact activities:

We will explain our science to the public via the media, public science events including literary/book festivals and through UCAS visit days. We showcase research in the Molecular Ecology lab to over 1000 visitors to the department every year, showing them how genomics tools and techniques can be used to address ecological questions. Biology students should also be beneficiaries of the research. Previous research from the team has featured in biology textbooks and we will promote the inclusion of this research in future editions.

Wider commercialisation of a SNP chip.
The SNP chip we have developed will be tested in multiple populations. Having evaluated its applicability to their own populations, researchers leading other great tit long-term projects will be able to purchase chips via the provider Illumina, a global company with a UK headquarters.

Our research team will continue to ensure that we promote our NERC-funded science with support from the University's Press Office.
 
Description We have generated a high density SNP chip (a DNA profiling tool) for great tits that has been used to examine populations from across Europe. The tool contains half a million markers and therefore is one of the most comprehensive genetic tools for studying natural vertebrate populations. Analyses are ongoing, but it appears that great tits experience large amounts of gene flow between populations, including the UK and mainland Europe. We identified regions of the genome responsible for the evolution of longer bills in UK populations; the publication describing this research has recevied a lot of attention from the media.
Exploitation Route Our collaborators in the Netherlands have subsequently ordered and used the SNP chip that we developed, and so our findings are being put to use in studies of how species adapt to climate change. They spent approx 400K Euro on new chips from our supplier, and so our findings contributed to the biotech economy.
Sectors Environment

Manufacturing

including Industrial Biotechology

 
Description Our collaborators in the Netherlands are using the DNA profiling chip that we created during this project. They have spent approximately 400K Euro on the chip, in order to pursue their research into how great tits are adapting to climate change.
First Year Of Impact 2015
Sector Education,Manufacturing, including Industrial Biotechology
Impact Types Economic

 
Title Data from: A high density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour 
Description High density SNP microarrays ('SNP chips') are a rapid, accurate and efficient method for genotyping several hundred thousand polymorphisms in large numbers of individuals. While SNP chips are routinely used in human genetics and in animal and plant breeding, they are less widely used in evolutionary and ecological research. In this paper we describe the development and application of a high density Affymetrix Axiom chip with around 500 000 SNPs, designed to perform genomics studies of great tit (Parus major) populations. We demonstrate that the per-SNP genotype error rate is well below 1% and that the chip can also be used to identify structural or copy number variation (CNVs). The chip is used to explore the genetic architecture of exploration behaviour (EB), a personality trait that has been widely studied in great tits and other species. No SNPs reached genome-wide significance, including at DRD4, a candidate gene. However, EB is heritable and appears to have a polygenic architecture. Researchers developing similar SNP chips may note: (i) SNPs previously typed on alternative platforms are more likely to be converted to working assays, (ii) detecting SNPs by more than one pipeline, and in independent datasets, ensures a high proportion of working assays, (iii) allele frequency ascertainment bias is minimised by performing SNP discovery in individuals from multiple populations and (iv) samples with the lowest call rates tend to also have the greatest genotyping error rates. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.7d467b6
 
Title Data from: Recent natural selection causes adaptive evolution of an avian polygenic trait 
Description We used extensive data from a long-term study of great tits (Parus major) in the United Kingdom and Netherlands to better understand how genetic signatures of selection translate into variation in fitness and phenotypes. We found that genomic regions under differential selection contained candidate genes for bill morphology and used genetic architecture analyses to confirm that these genes, especially the collagen gene COL4A5, explained variation in bill length. COL4A5 variation was associated with reproductive success, which, combined with spatiotemporal patterns of bill length, suggested ongoing selection for longer bills in the United Kingdom. Last, bill length and COL4A5 variation were associated with usage of feeders, suggesting that longer bills may have evolved in the United Kingdom as a response to supplementary feeding. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.p03j0
 
Title The genomics of adaptation to climate in European great tit (Parus major) populations 
Description The recognition that climate change is occurring at an unprecedented rate means that there is increased urgency in understanding how organisms can adapt to a changing environment. Wild great tit (Parus major) populations represent an attractive ecological model system to understand the genomics of climate adaptation. They are widely distributed across Eurasia and they have been documented to respond to climate change. We performed a Bayesian genome-environment analysis, by combining local climate data with SNP genotype data from 20 European populations (broadly spanning the species' continental range). We found 36 unique putative climate adaptation genes that were associated with variation in climate. Following an enrichment analysis of biological process Gene Ontology (GO) terms, we identified over-represented terms and pathways among the genes putatively under selection for climate adaptation. Because many different genes and GO terms are associated with climate variables, it seems likely that climate adaptation is polygenic and genetically complex. Our findings also suggest that geographical climate adaptation has been occurring since great tits left their Southern European refugia at the end of the last ice age. Finally, we show that substantial climate-associated genetic variation remains, which will be essential for adaptation to future changes. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.vt4b8gtxd
 
Description Great tit HapMap Consortium 
Organisation Eotvos Lorand University
Country Hungary 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Hokkaido University
Country Japan 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Jagiellonian University
Country Poland 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Max Planck Society
Department Max Planck Institute for Ornithology
Country Germany 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Moscow State University
Country Russian Federation 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation National Center for Scientific Research (Centre National de la Recherche Scientifique CNRS)
Department IN2P3 CNRS
Country France 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation National Center for Scientific Research (Centre National de la Recherche Scientifique CNRS)
Department UMR CNRS 5558 Laboratoire de Biométrie et Biologie Évolutive
Country France 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Netherlands Institute of Ecology
Country Netherlands 
Sector Charity/Non Profit 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Norwegian Institute for Nature Research
Country Norway 
Sector Public 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Palacky University
Country Czech Republic 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Polytechnic University of Valencia
Country Spain 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Antwerp
Country Belgium 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Bern
Country Switzerland 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Coimbra
Country Portugal 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of East Anglia
Country United Kingdom 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Glasgow
Country United Kingdom 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Groningen
Country Netherlands 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Groningen
Country Netherlands 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Natural Resources and Life Sciences
Country Austria 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Oslo
Country Norway 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Oulu
Country Finland 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Oxford
Country United Kingdom 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Tartu
Country Estonia 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Tartu
Country Estonia 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Turku
Country Finland 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation University of Zurich
Country Switzerland 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description Great tit HapMap Consortium 
Organisation Wageningen University & Research
Country Netherlands 
Sector Academic/University 
PI Contribution I led a team of researchers interested in studying the population genetics of great tits. The consortium uses data from over 20 study populations across Europe and into Asia.
Collaborator Contribution Blood and/or DNA samples from nest box populations of great tits.
Impact Publications listed in relevant section
Start Year 2014
 
Description BBC Radio World Service interview 
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 I conducted an interview on BBC Radio World Service, about our research on the evolution of bird bills
Year(s) Of Engagement Activity 2017
 
Description Presentation at school 6th Form STEM club 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Presentation on long term ecological studies of wild animals at Tapton School (6th Form STEM club)
Year(s) Of Engagement Activity 2018
 
Description Radio interview for BBC Radio 4 - Six o'clock news 
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 Media (as a channel to the public)
Results and Impact I was interviewed on national radio, during a peak slot, about our work on the evolution of bird bill lengths
Year(s) Of Engagement Activity 2017
 
Description Spoke at public event - Pint Of Science 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Approximately 60 people attended a talk I gave at The Sheffield Tap, as part of the nationwide 'Pint of Science' event. I spoke about the value of long term individual-based studies of animal populations, and why they inspire so many biologists.
Year(s) Of Engagement Activity 2017
URL https://pintofscience.co.uk/
 
Description Widespread print and online coverage of our research on the evolution of bird bills 
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 Our paper published in Science recevied international attention, and was featured in UK (The Times, The Telegraph, The Guardian, The Daily Mail, BBC News, regional papers) and international (Washington Post, Yahoo, Forbes, Eureka Alerts!, National Geographic) news outlets.
Year(s) Of Engagement Activity 2017