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

Lewis G. Spurgin; Mirte Bosse; Frank Adriaensen; Tamer Albayrak; Christos Barboutis; Eduardo Belda; Andrey Bushuev; Jacopo G. Cecere; Anne Charmantier; Mariusz Cichon; Niels J. Dingemanse; Blandine Doligez; Tapio Eeva; Kjell Einar Erikstad; Vyacheslav Fedorov; Matteo Griggio; Dieter Heylen; Sabine Hille; Camilla A. Hinde; Elena Ivankina; Bart Kempenaers; Anvar Kerimov; Milos Krist; Laura Kvist; Veronika N. Laine; Raivo Mänd; Erik Matthysen; Ruedi Nager; Boris P. Nikolov; A. Claudia Norte; Markku Orell; Jenny Ouyang; Gergana Petrova-Dinkova; Heinz Richner; Diego Rubolini; Tore Slagsvold; Vallo Tilgar; János Török; Barbara Tschirren; Csongor I. Vágási; Teru Yuta; Martien A. M. Groenen; Marcel E. Visser; Kees van Oers; Ben C. Sheldon; Jon Slate

doi:10.1101/561399

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

Lewis G. Spurgin, Mirte Bosse, Frank Adriaensen, Tamer Albayrak, Christos Barboutis, Eduardo Belda, Andrey Bushuev, Jacopo G. Cecere, Anne Charmantier, Mariusz Cichon, Niels J. Dingemanse, Blandine Doligez, Tapio Eeva, Kjell Einar Erikstad, Vyacheslav Fedorov, Matteo Griggio, Dieter Heylen, Sabine Hille, Camilla A. Hinde, Elena IvankinaBart Kempenaers, Anvar Kerimov, Milos Krist, Laura Kvist, Veronika N. Laine, Raivo Mänd, Erik Matthysen, Ruedi Nager, Boris P. Nikolov, A. Claudia Norte, Markku Orell, Jenny Ouyang, Gergana Petrova-Dinkova, Heinz Richner, Diego Rubolini, Tore Slagsvold, Vallo Tilgar, János Török, Barbara Tschirren, Csongor I. Vágási, Teru Yuta, Martien A. M. Groenen, Marcel E. Visser, Kees van Oers, Ben C. Sheldon, Jon Slate

Work enabled by Edinburgh Genomics

Research output: Working paper › Preprint

Abstract / Description of output

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out 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 almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, 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 rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

Original language	English
Publisher	bioRxiv
DOIs	https://doi.org/10.1101/561399
Publication status	Published - 9 Dec 2020

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10.1101/561399Licence: Creative Commons: Attribution-NonCommercial-NoDerivatives (CC BY-NC-ND)

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Spurgin, L. G., Bosse, M., Adriaensen, F., Albayrak, T., Barboutis, C., Belda, E., Bushuev, A., Cecere, J. G., Charmantier, A., Cichon, M., Dingemanse, N. J., Doligez, B., Eeva, T., Erikstad, K. E., Fedorov, V., Griggio, M., Heylen, D., Hille, S., Hinde, C. A., ... Slate, J. (2020). The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird. bioRxiv. https://doi.org/10.1101/561399

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

abstract = "A major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out 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 almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, 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 rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.",

author = "Spurgin, {Lewis G.} and Mirte Bosse and Frank Adriaensen and Tamer Albayrak and Christos Barboutis and Eduardo Belda and Andrey Bushuev and Cecere, {Jacopo G.} and Anne Charmantier and Mariusz Cichon and Dingemanse, {Niels J.} and Blandine Doligez and Tapio Eeva and Erikstad, {Kjell Einar} and Vyacheslav Fedorov and Matteo Griggio and Dieter Heylen and Sabine Hille and Hinde, {Camilla A.} and Elena Ivankina and Bart Kempenaers and Anvar Kerimov and Milos Krist and Laura Kvist and Laine, {Veronika N.} and Raivo M{\"a}nd and Erik Matthysen and Ruedi Nager and Nikolov, {Boris P.} and Norte, {A. Claudia} and Markku Orell and Jenny Ouyang and Gergana Petrova-Dinkova and Heinz Richner and Diego Rubolini and Tore Slagsvold and Vallo Tilgar and J{\'a}nos T{\"o}r{\"o}k and Barbara Tschirren and V{\'a}g{\'a}si, {Csongor I.} and Teru Yuta and Groenen, {Martien A. M.} and Visser, {Marcel E.} and Oers, {Kees van} and Sheldon, {Ben C.} and Jon Slate",

year = "2020",

month = dec,

day = "9",

doi = "10.1101/561399",

language = "English",

publisher = "bioRxiv",

type = "WorkingPaper",

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Spurgin, LG, Bosse, M, Adriaensen, F, Albayrak, T, Barboutis, C, Belda, E, Bushuev, A, Cecere, JG, Charmantier, A, Cichon, M, Dingemanse, NJ, Doligez, B, Eeva, T, Erikstad, KE, Fedorov, V, Griggio, M, Heylen, D, Hille, S, Hinde, CA, Ivankina, E, Kempenaers, B, Kerimov, A, Krist, M, Kvist, L, Laine, VN, Mänd, R, Matthysen, E, Nager, R, Nikolov, BP, Norte, AC, Orell, M, Ouyang, J, Petrova-Dinkova, G, Richner, H, Rubolini, D, Slagsvold, T, Tilgar, V, Török, J, Tschirren, B, Vágási, CI, Yuta, T, Groenen, MAM, Visser, ME, Oers, KV, Sheldon, BC & Slate, J 2020 'The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird' bioRxiv. https://doi.org/10.1101/561399

TY - UNPB

T1 - The great tit HapMap project

T2 - A continental-scale analysis of genomic variation in a songbird

AU - Spurgin, Lewis G.

AU - Bosse, Mirte

AU - Adriaensen, Frank

AU - Albayrak, Tamer

AU - Barboutis, Christos

AU - Belda, Eduardo

AU - Bushuev, Andrey

AU - Cecere, Jacopo G.

AU - Charmantier, Anne

AU - Cichon, Mariusz

AU - Dingemanse, Niels J.

AU - Doligez, Blandine

AU - Eeva, Tapio

AU - Erikstad, Kjell Einar

AU - Fedorov, Vyacheslav

AU - Griggio, Matteo

AU - Heylen, Dieter

AU - Hille, Sabine

AU - Hinde, Camilla A.

AU - Ivankina, Elena

AU - Kempenaers, Bart

AU - Kerimov, Anvar

AU - Krist, Milos

AU - Kvist, Laura

AU - Laine, Veronika N.

AU - Mänd, Raivo

AU - Matthysen, Erik

AU - Nager, Ruedi

AU - Nikolov, Boris P.

AU - Norte, A. Claudia

AU - Orell, Markku

AU - Ouyang, Jenny

AU - Petrova-Dinkova, Gergana

AU - Richner, Heinz

AU - Rubolini, Diego

AU - Slagsvold, Tore

AU - Tilgar, Vallo

AU - Török, János

AU - Tschirren, Barbara

AU - Vágási, Csongor I.

AU - Yuta, Teru

AU - Groenen, Martien A. M.

AU - Visser, Marcel E.

AU - Oers, Kees van

AU - Sheldon, Ben C.

AU - Slate, Jon

PY - 2020/12/9

Y1 - 2020/12/9

N2 - A major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out 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 almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, 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 rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

AB - A major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out 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 almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, 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 rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

U2 - 10.1101/561399

DO - 10.1101/561399

M3 - Preprint

BT - The great tit HapMap project

PB - bioRxiv

ER -

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

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