Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations

Authors

  • Jakob C. Mueller,

    Corresponding author
    1. Department of Behavioural Ecology & Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany
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  • Peter Korsten,

    1. Department of Behavioural Ecology & Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany
    Current affiliation:
    1. Centre for Ecological and Evolutionary Studies, Behavioural Ecology and Self-Organization group, University of Groningen, Groningen, The Netherlands
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  • Christine Hermannstaedter,

    1. Department of Behavioural Ecology & Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany
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  • Thomas Feulner,

    1. Clinic for Psychiatry and Psychotherapy, University of Saarland, Homburg/Saar, Germany
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  • Niels J. Dingemanse,

    1. Research Group “Evolutionary Ecology of Variation”, Max Planck Institute for Ornithology, Seewiesen, Germany
    2. Department Biologie II, Ludwig Maximilians University of Munich, Planegg-Martinsried, Germany
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  • Erik Matthysen,

    1. Evolutionary Ecology Group, Department of Biology, University of Antwerp, Wilrijk, Belgium
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  • Kees van Oers,

    1. Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
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  • Thijs van Overveld,

    1. Evolutionary Ecology Group, Department of Biology, University of Antwerp, Wilrijk, Belgium
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  • Samantha C. Patrick,

    1. Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK
    Current affiliation:
    1. Centre d'Etudes Biologiques de Chizé, CNRS, Villiers-en-Bois, France
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  • John L. Quinn,

    1. Edward Grey Institute, Department of Zoology, University of Oxford, Oxford, UK
    Current affiliation:
    1. School of BEES, University College Cork, Cork, Ireland
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  • Matthias Riemenschneider,

    1. Clinic for Psychiatry and Psychotherapy, University of Saarland, Homburg/Saar, Germany
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  • Joost M. Tinbergen,

    1. Animal Ecology Group, University of Groningen, Groningen, The Netherlands
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  • Bart Kempenaers

    1. Department of Behavioural Ecology & Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany
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Abstract

The assessment of genetic architecture and selection history in genes for behavioural traits is fundamental to our understanding of how these traits evolve. The dopamine receptor D4 (DRD4) gene is a prime candidate for explaining genetic variation in novelty seeking behaviour, a commonly assayed personality trait in animals. Previously, we showed that a single nucleotide polymorphism in exon 3 of this gene is associated with exploratory behaviour in at least one of four Western European great tit (Parus major) populations. These heterogeneous association results were explained by potential variable linkage disequilibrium (LD) patterns between this marker and the causal variant or by other genetic or environmental differences among the populations. Different adaptive histories are further hypothesized to have contributed to these population differences. Here, we genotyped 98 polymorphisms of the complete DRD4 gene including the flanking regions for 595 individuals of the four populations. We show that the LD structure, specifically around the original exon 3 SNP is conserved across the four populations and does not explain the heterogeneous association results. Study-wide significant associations with exploratory behaviour were detected in more than one haplotype block around exon 2, 3 and 4 in two of the four tested populations with different allele effect models. This indicates genetic heterogeneity in the association between multiple DRD4 polymorphisms and exploratory behaviour across populations. The association signals were in or close to regions with signatures of positive selection. We therefore hypothesize that variation in exploratory and other dopamine-related behaviour evolves locally by occasional adaptive shifts in the frequency of underlying genetic variants.

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