The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird

Lewis G Spurgin^{1

2}, Mirte Bosse^{3

4

5}, Frank Adriaensen⁶, Tamer Albayrak^{7

8}, Christos Barboutis⁹, Eduardo Belda¹⁰, Andrey Bushuev¹¹, Jacopo G Cecere¹², Anne Charmantier¹³, Mariusz Cichon¹⁴, Niels J Dingemanse¹⁵, Blandine Doligez^{16

17}, Tapio Eeva¹⁸, Kjell Einar Erikstad¹⁹, Vyacheslav Fedorov¹¹, Matteo Griggio²⁰, Dieter Heylen^{2

6

21}, Sabine Hille²², Camilla A Hinde²³, Elena Ivankina²⁴, Bart Kempenaers²⁵, Anvar Kerimov¹¹, Milos Krist²⁶, Laura Kvist²⁷, Veronika N Laine^{3

28}, Raivo Mänd²⁹, Erik Matthysen⁶, Ruedi Nager³⁰, Boris P Nikolov³¹, Ana Claudia Norte³², Markku Orell²⁷, Jenny Ouyang³³, Gergana Petrova-Dinkova³¹, Heinz Richner³⁴, Diego Rubolini³⁵, Tore Slagsvold³⁶, Vallo Tilgar²⁹, János Török³⁷, Barbara Tschirren³⁸, Csongor I Vágási³⁹, Teru Yuta⁴⁰, Martien A M Groenen⁴, Marcel E Visser^{3

4

41}, Kees van Oers³, Ben C Sheldon², Jon Slate⁴²

Affiliations

¹ School of Biological Sciences, Norwich Research Park, University of East Anglia, Norwich, UK.
² Department of Biology, Edward Grey Institute, University of Oxford, Oxford, UK.
³ Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
⁴ Animal Breeding and Genomics, Wageningen University and Research, Wageningen, The Netherlands.
⁵ Department of Ecological Science, Animal Ecology Group, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁶ Evolutionary Ecology Group, Department of Biology, University of Antwerp, Antwerp, Belgium.
⁷ Department of Biology, Science and art Faculty, Mehmet Akif Ersoy University, Istiklal Yerleskesi, Burdur, Turkey.
⁸ Biology Education, Buca Faculty of Education, Mathematics and Science Education, Dokuz Eylül University, İzmir, Turkey.
⁹ Hellenic Ornithological Society/BirdLife Greece, Athens, Greece.
¹⁰ Institut d'Investigació per a la Gestió Integrada de Zones Costaneres, Campus de Gandia, Universitat Politècnica de València, València, Spain.
¹¹ Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia.
¹² Area Avifauna Migratrice, Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA), Ozzano Emilia, Italy.
¹³ CEFE, Univ. Montpellier, CNRS, EPHE, IRD, Montpellier, France.
¹⁴ Institute of Environmental Sciences, Jagiellonian University, Kraków, Poland.
¹⁵ Behavioural Ecology, Faculty of Biology, LMU München, Planegg-Martinsried, Germany.
¹⁶ UMR CNRS 5558-LBBE, Biométrie et Biologie Évolutive, Villeurbanne, France.
¹⁷ Department of Ecology and Evolution, Animal Ecology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
¹⁸ Department of Biology, University of Turku, Turku, Finland.
¹⁹ Norwegian Institute for Nature Research, FRAM-High North Research Centre for Climate and the Environment, Tromsø, Norway.
²⁰ Department of Biology, University of Padova, Padova, Italy.
²¹ Interuniversity Institute for Biostatistics and Statistical Bioinformatics, Hasselt University, Diepenbeek, Belgium.
²² Institute of Wildlife Biology and Game Management, University of Natural Resources and Life Science, Vienna, Austria.
²³ Behavioural Ecology Group, Department of Life Sciences, Anglia Ruskin University, Cambridgeshire, UK.
²⁴ Faculty of Biology, Zvenigorod Biological Station, Lomonosov Moscow State University, Moscow, Russia.
²⁵ Department of Ornithology, Max Planck Institute for Biological Intelligence, Seewiesen, Germany.
²⁶ Department of Zoology, Faculty of Science, Palacký University, Olomouc, Czech Republic.
²⁷ Department of Ecology and Genetics, University of Oulu, Oulu, Finland.
²⁸ Zoology Unit, Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland.
²⁹ Department of Zoology, University of Tartu, Tartu, Estonia.
³⁰ School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow, UK.
³¹ Bulgarian Ornithological Centre, Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria.
³² MARE - Marine and Environmental Sciences Centre, Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal.
³³ University of Nevada, Reno, Nevada, USA.
³⁴ Evolutionary Ecology Lab, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.
³⁵ Dipartimento di Scienze e Politiche Ambientali, Università Degli Studi di Milano, Milan, Italy.
³⁶ Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway.
³⁷ Behavioural Ecology Group, Department of Systematic Zoology and Ecology, ELTE Eötvös Loránd University, Budapest, Hungary.
³⁸ Centre for Ecology and Conservation, University of Exeter, Penryn, UK.
³⁹ Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeș-Bolyai University, Cluj-Napoca, Romania.
⁴⁰ Yamashina Institute for Ornithology, Abiko, Japan.
⁴¹ Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, the Netherlands.
⁴² School of Biosciences, University of Sheffield, Sheffield, UK.

PMID: 38747336
DOI: 10.1111/1755-0998.13969

Free article

The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird

Lewis G Spurgin et al. Mol Ecol Resour. 2024 Jul.

Free article

. 2024 Jul;24(5):e13969.

doi: 10.1111/1755-0998.13969. Epub 2024 May 15.

Authors

Affiliations

¹ School of Biological Sciences, Norwich Research Park, University of East Anglia, Norwich, UK.
² Department of Biology, Edward Grey Institute, University of Oxford, Oxford, UK.
³ Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.
⁴ Animal Breeding and Genomics, Wageningen University and Research, Wageningen, The Netherlands.
⁵ Department of Ecological Science, Animal Ecology Group, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁶ Evolutionary Ecology Group, Department of Biology, University of Antwerp, Antwerp, Belgium.
⁷ Department of Biology, Science and art Faculty, Mehmet Akif Ersoy University, Istiklal Yerleskesi, Burdur, Turkey.
⁸ Biology Education, Buca Faculty of Education, Mathematics and Science Education, Dokuz Eylül University, İzmir, Turkey.
⁹ Hellenic Ornithological Society/BirdLife Greece, Athens, Greece.
¹⁰ Institut d'Investigació per a la Gestió Integrada de Zones Costaneres, Campus de Gandia, Universitat Politècnica de València, València, Spain.
¹¹ Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia.
¹² Area Avifauna Migratrice, Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA), Ozzano Emilia, Italy.
¹³ CEFE, Univ. Montpellier, CNRS, EPHE, IRD, Montpellier, France.
¹⁴ Institute of Environmental Sciences, Jagiellonian University, Kraków, Poland.
¹⁵ Behavioural Ecology, Faculty of Biology, LMU München, Planegg-Martinsried, Germany.
¹⁶ UMR CNRS 5558-LBBE, Biométrie et Biologie Évolutive, Villeurbanne, France.
¹⁷ Department of Ecology and Evolution, Animal Ecology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
¹⁸ Department of Biology, University of Turku, Turku, Finland.
¹⁹ Norwegian Institute for Nature Research, FRAM-High North Research Centre for Climate and the Environment, Tromsø, Norway.
²⁰ Department of Biology, University of Padova, Padova, Italy.
²¹ Interuniversity Institute for Biostatistics and Statistical Bioinformatics, Hasselt University, Diepenbeek, Belgium.
²² Institute of Wildlife Biology and Game Management, University of Natural Resources and Life Science, Vienna, Austria.
²³ Behavioural Ecology Group, Department of Life Sciences, Anglia Ruskin University, Cambridgeshire, UK.
²⁴ Faculty of Biology, Zvenigorod Biological Station, Lomonosov Moscow State University, Moscow, Russia.
²⁵ Department of Ornithology, Max Planck Institute for Biological Intelligence, Seewiesen, Germany.
²⁶ Department of Zoology, Faculty of Science, Palacký University, Olomouc, Czech Republic.
²⁷ Department of Ecology and Genetics, University of Oulu, Oulu, Finland.
²⁸ Zoology Unit, Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland.
²⁹ Department of Zoology, University of Tartu, Tartu, Estonia.
³⁰ School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow, UK.
³¹ Bulgarian Ornithological Centre, Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria.
³² MARE - Marine and Environmental Sciences Centre, Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal.
³³ University of Nevada, Reno, Nevada, USA.
³⁴ Evolutionary Ecology Lab, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.
³⁵ Dipartimento di Scienze e Politiche Ambientali, Università Degli Studi di Milano, Milan, Italy.
³⁶ Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway.
³⁷ Behavioural Ecology Group, Department of Systematic Zoology and Ecology, ELTE Eötvös Loránd University, Budapest, Hungary.
³⁸ Centre for Ecology and Conservation, University of Exeter, Penryn, UK.
³⁹ Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeș-Bolyai University, Cluj-Napoca, Romania.
⁴⁰ Yamashina Institute for Ornithology, Abiko, Japan.
⁴¹ Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, the Netherlands.
⁴² School of Biosciences, University of Sheffield, Sheffield, UK.

PMID: 38747336
DOI: 10.1111/1755-0998.13969

Abstract

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (F_ST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Keywords: adaptation; birds; ecological genetics; genomics/proteomics; molecular evolution; population genetics – empirical.

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The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird

Affiliations

The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird

Authors

Affiliations

Abstract

References

REFERENCES

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Miscellaneous