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The genomic basis of color pattern polymorphism in the harlequin ladybird

Gautier Mathieu, Yamaguchi Junichi, Foucaud Julien, Loiseau Anne, Ausset Aurélien, Facon Benoît, Gschloessl Bernhard, Lagnel Jacques, Loire Etienne, Parrinello Hugues, Severac Dany, Lopez-Roques Céline, Donnadieu Cécile, Manno Maxime, Berges Hélène, Gharbi Karim, Lawson-Handley Lori, Zang Lian-Sheng, Vogel Heiko, Estoup Arnaud, Prud'homme Benjamin. 2018. The genomic basis of color pattern polymorphism in the harlequin ladybird. Current Biology, 28 (20):e7 : pp. 3296-3302.

Journal article ; Article de recherche ; Article de revue à facteur d'impact
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Quartile : Outlier, Sujet : BIOCHEMISTRY & MOLECULAR BIOLOGY / Quartile : Q1, Sujet : CELL BIOLOGY

Liste HCERES des revues (en SHS) : oui

Thème(s) HCERES des revues (en SHS) : Anthropologie-Ethnologie; Psychologie-éthologie-ergonomie

Abstract : Many animal species comprise discrete phenotypic forms. A common example in natural populations of insects is the occurrence of different color patterns, which has motivated a rich body of ecological and genetic research [1, 2, 3, 4, 5, 6]. The occurrence of dark, i.e., melanic, forms displaying discrete color patterns is found across multiple taxa, but the underlying genomic basis remains poorly characterized. In numerous ladybird species (Coccinellidae), the spatial arrangement of black and red patches on adult elytra varies wildly within species, forming strikingly different complex color patterns [7, 8]. In the harlequin ladybird, Harmonia axyridis, more than 200 distinct color forms have been described, which classic genetic studies suggest result from allelic variation at a single, unknown, locus [9, 10]. Here, we combined whole-genome sequencing, population-based genome-wide association studies, gene expression, and functional analyses to establish that the transcription factor Pannier controls melanic pattern polymorphism in H. axyridis. We show that pannier is necessary for the formation of melanic elements on the elytra. Allelic variation in pannier leads to protein expression in distinct domains on the elytra and thus determines the distinct color patterns in H. axyridis. Recombination between pannier alleles may be reduced by a highly divergent sequence of ∼170 kb in the cis-regulatory regions of pannier, with a 50 kb inversion between color forms. This most likely helps maintain the distinct alleles found in natural populations. Thus, we propose that highly variable discrete color forms can arise in natural populations through cis-regulatory allelic variation of a single gene.

Mots-clés Agrovoc : Coccinellidae

Mots-clés libres : Genomics, Ecology

Classification Agris : L10 - Animal genetics and breeding
L20 - Animal ecology

Champ stratégique Cirad : Axe 6 (2014-2018) - Sociétés, natures et territoires

Agence(s) de financement européenne(s) : European Commission

Programme de financement européen : FP7

Projet(s) de financement européen(s) : Evolution of a Drosophila wing pigmentation spot, a sexual communication system

Auteurs et affiliations

  • Gautier Mathieu, INRA (FRA)
  • Yamaguchi Junichi, Université Aix-Marseille (FRA)
  • Foucaud Julien, INRA (FRA)
  • Loiseau Anne, INRA (FRA)
  • Ausset Aurélien, INRA (FRA)
  • Facon Benoît, INRA (FRA)
  • Gschloessl Bernhard, INRA (FRA)
  • Lagnel Jacques, INRA (FRA)
  • Loire Etienne, CIRAD-BIOS-UMR ASTRE (FRA)
  • Parrinello Hugues, CNRS (FRA)
  • Severac Dany, CNRS (FRA)
  • Lopez-Roques Céline, INRA (FRA)
  • Donnadieu Cécile, INRA (FRA)
  • Manno Maxime, INRA (FRA)
  • Berges Hélène, INRA (FRA)
  • Gharbi Karim, University of Edinburgh (GBR)
  • Lawson-Handley Lori, University of Hull (GBR)
  • Zang Lian-Sheng, Jilin University (CHN)
  • Vogel Heiko, MPIZ (DEU)
  • Estoup Arnaud, INRA (FRA) - auteur correspondant
  • Prud'homme Benjamin, Université Aix-Marseille (FRA) - auteur correspondant

Source : Cirad-Agritrop (https://agritrop.cirad.fr/590535/)

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