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Curr Biol. 2018 Oct 22;28(20):3296-3302.e7. doi: 10.1016/j.cub.2018.08.023. Epub 2018 Aug 23.

The Genomic Basis of Color Pattern Polymorphism in the Harlequin Ladybird.

Author information

1
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Université de Montpellier, Montpellier, France.
2
Aix Marseille Université, CNRS, IBDM, Marseille, France.
3
MGX, Biocampus Montpellier, CNRS, INSERM, Université de Montpellier, Montpellier, France.
4
INRA, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France.
5
INRA, Centre National de Ressources Génomiques Végétales, 31326 Castanet-Tolosan, France.
6
Edinburgh Genomics, University of Edinburgh, Edinburgh, UK.
7
Evolutionary and Environmental Genomics Group, School of Environmental Sciences, University of Hull, Hull HU6 7RX, UK.
8
Institute of Biological Control, Jilin Agricultural University, Changchun, China.
9
Department of Entomology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
10
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Université de Montpellier, Montpellier, France. Electronic address: arnaud.estoup@inra.fr.
11
Aix Marseille Université, CNRS, IBDM, Marseille, France. Electronic address: benjamin.prudhomme@univ-amu.fr.

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 [1-6]. 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.

KEYWORDS:

Harmonia axyridis; cis-regulation; color forms; de novo genome assemblies; evolutionary genetics; gene expression; genome-wide association study; harlequin ladybird; inversion; melanic pattern polymorphism

PMID:
30146156
PMCID:
PMC6203698
DOI:
10.1016/j.cub.2018.08.023
[Indexed for MEDLINE]
Free PMC Article

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