The Genomic Basis of Color Pattern Polymorphism in the Harlequin Ladybird

• Published in: Current biology Vol. 28; no. 20; pp. 3296 - 3302.e7
• Main Authors: 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
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 22-10-2018; Elsevier; Cell Press
• Subjects: Animals; cis-regulation; Coleoptera - genetics; Coleoptera - physiology; Color; color forms; de novo genome assemblies; evolutionary genetics; Female; gene expression; Gene Expression Regulation; Genome, Insect; Genome-Wide Association Study; Genomics; harlequin ladybird; Harmonia axyridis; inversion; Life Sciences; Male; melanic pattern polymorphism; Pigmentation - genetics; Pigments, Biological - metabolism; Polymorphism, Single Nucleotide; Vegetal Biology; melanic pattern polymorphism; inversion; de novo genome assemblies; harlequin ladybird; genome-wide association study; cis-regulation; Harmonia axyridis; gene expression; color forms; evolutionary genetics; harmonia axyridis; polymorphism; coccinelle; étude d'association pangénomique; allèle; approche génomique; phénotype; polymorphisme; génétique évolutive
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2018.08.023

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.
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•The harlequin ladybird displays various color pattern forms in natural populations•The transcription factor Pannier controls this color polymorphism•Pannier is essential for the formation of melanic elements on the elytra•The cis-regulatory regions of pannier have diverged extensively among color forms
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.