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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, Benoit; Gschloessl, Bernhard; Lagnel, Jacques; Loire, Etienne; Parrinello, Hugues; Severac, Dany; Lopez-Roques, Celine; Donnadieu, Cecile; Manno, Maxime; Berges, Helene; Gharbi, Karim; Lawson-Handley, Lori; Zang, Lian-Sheng; Vogel, Heiko; Estoup, Arnaud; Prud'homme, Benjamin

Authors

Mathieu Gautier

Junichi Yamaguchi

Julien Foucaud

Anne Loiseau

Aurélien Ausset

Benoit Facon

Bernhard Gschloessl

Jacques Lagnel

Etienne Loire

Hugues Parrinello

Dany Severac

Celine Lopez-Roques

Cecile Donnadieu

Maxime Manno

Helene Berges

Karim Gharbi

Lori Lawson-Handley

Lian-Sheng Zang

Heiko Vogel

Arnaud Estoup

Benjamin Prud'homme



Abstract

© 2018 The Authors 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 [1–6]. 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. More than 200 distinct color forms have been described in natural populations of the harlequin ladybird, Harmonia axyridis. Gautier et al. show that this variation is controlled by the transcription factor Pannier. Pannier is necessary to produce black pigment, and its expression pattern prefigures the coloration pattern in each color form.

Journal Article Type Article
Publication Date Oct 22, 2018
Journal Current Biology
Print ISSN 0960-9822
Publisher Elsevier
Peer Reviewed Peer Reviewed
Volume 28
Issue 20
Pages 3296-3302.e7
APA6 Citation Gautier, M., Yamaguchi, J., Foucaud, J., Loiseau, A., Ausset, A., Facon, B., …Prud'homme, B. (2018). The genomic basis of color pattern polymorphism in the Harlequin ladybird. Current biology : CB, 28(20), 3296-3302.e7. doi:10.1016/j.cub.2018.08.023
DOI https://doi.org/10.1016/j.cub.2018.08.023
Keywords General Biochemistry, Genetics and Molecular Biology; General Agricultural and Biological Sciences
Publisher URL https://www.sciencedirect.com/science/article/pii/S0960982218310686?via%3Dihub
Copyright Statement © 2018 The Authors

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

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Copyright Statement
© 2018 The Authors

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.



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