Sex‐Specific doublesex Regulation Targeting the Color‐Patterning Gene h Underlies the Evolution of Wing Sexual Dimorphism in the Harlequin Ladybug Harmonia axyridis - Research Article

Sep 29, 2026

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Organisms exhibit diverse sexual dimorphism shaped by sexual selection, yet the evolution of the regulatory systems that control gain or loss of such traits remains unclear. This study analyzes strain-specific sexual dimorphism in elytral color patterns of the harlequin ladybug Harmonia axyridis. Using comparative ATAC-seq and mechanistic focus on doublesex (dsx), it shows dsx controls color-pattern dimorphism by negatively modulating male black-spot size via transcriptional regulation of gene h. Results indicate sexual dimorphism evolves from balancing novel CREs and Dsx-binding motif density.

LanguageEnglish

CategoryResearch & Report

FormatPDF

Pages15

Reading Time38 min

AccessFree to download

Abstract

Summary

Introduction

Secondary sexual traits and sexual dimorphism

dsx as a conserved sex differentiation regulator

Need for comparative analyses across insect lineages

Evolution & Development RESEARCH ARTICLE Sex‐Specific doublesex Regulation Targeting the Color‐Patterning Gene h Underlies the Evolution of Wing Sexual Dimorphism in the Harlequin Ladybug Harmonia axyridis Soichi Yeki1,2 | Kagayaki Kato3,4 | Shinichi Morita4,5 | Kenji Shimomura6 | Teruyuki Niimi4,5 | Norihide Hinomoto2 | Takaaki Daimon1 | Toshiya Ando1,4,5,7,8 1Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, Kyoto, Japan | 2Division of Environmental Science and Technology, Graduate School of Agriculture, Kyoto University, Kyoto, Kyoto, Japan | 3Optics and Imaging Facility, Trans‐Scale Biology Center, National Institute for Basic Biology, Okazaki, Aichi, Japan | 4Basic Biology Program, The Graduate University for Advanced Studies, SOKENDAI, Okazaki, Aichi, Japan | 5Division of Evolutionary Developmental Biology, National Institute for Basic Biology, Okazaki, Aichi, Japan | 6Department of Chemistry for Life Sciences and Agriculture, Faculty of Life Sciences, Tokyo University of Agriculture, Setagaya‐ku, Tokyo, Japan | 7PRESTO, JST, Kawaguchi, Saitama, Japan | 8The Hakubi Center for Advanced Research, Kyoto University, Kyoto, Kyoto, Japan Correspondence: Toshiya Ando ([toshiya.ando.ca@gmail.com](toshiya.ando.ca@gmail.com)) Received: 6 August 2025 | Revised: 8 December 2025 | Accepted: 24 December 2025 Funding: JST SPRING, Grant/Award Number: JPMJSP2110; JST PRESTO, Grant/Award Number: JPMPR20K1; KAKENHI, Grant/Award Numbers: 18H04828, 19H01004, 20H04874, 23H02227, 20H03003, 23K27219, 25H01424 Keywords: ATAC‐seq | doublesex | ladybug | sexual dimorphism | wing color pattern ABSTRACT Organisms on Earth show various forms of sexual dimorphism, including ornaments, weapon traits, and pheromone glands, which have been acquired through sexual selection during evolution. Although the genetic basis of sexual traits has been investigated in diverse species, how the underlying regulatory systems evolve during the gain or loss of sexual dimorphism within a species remains poorly understood. To address this issue, we investigated the strain‐specific sexual dimorphism in elytral color patterns of the harlequin ladybug, Harmonia axyridis (H. axyridis), a species with over 200 color morphs. The most basal Red‐nSpots type color morph exhibits sexual dimorphism, whereas other derived color morphs have lost it. To investigate how this sexual dimorphism was lost during the evolution of novel color morphs, we investigated the genetic basis of sexual dimorphism by focusing on the master sex differentiation gene, doublesex (dsx) . We show that dsx regulates color pattern dimorphism by negatively modulating black spot size in males. This modulation is primarily mediated by the transcriptional regulation of the color patterning gene, h (Drosophila pannier ortholog) . Intraspecific comparative ATAC‐seq analysis of the pupal wings revealed that, at the h locus, not the absolute number of Dsx‐binding motifs but the proportion of open chromatin regions containing Dsx‐binding motifs relative to those lacking such motifs was reduced in strains that had lost sexual dimorphism and acquired novel color patterns, implying that sexual dimorphism evolves based on the balance between novel CREs and Dsx‐binding motif density. The present study provides a fundamental molecular framework for understanding how a secondary sexual trait evolves within H. axyridis. | Toshiya Ando is the lead contact. | | --- | | This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
© 2026 The Author(s) . Evolution & Development published by Wiley Periodicals LLC. | Evolution & Development, 2026; 28:e70028 1 of 15 [https://doi.org/10.1111/ede.70028](https://doi.org/10.1111/ede.70028) Summary doublesex regulates sexual dimorphism in elytral color patterns of Harmonia

FAQs

What question does the study address about sexual dimorphism evolution?

How regulatory systems evolve during the gain or loss of sexual dimorphism within a species, specifically in the context of harlequin ladybug color-pattern traits.

How does dsx influence wing or elytral color-pattern dimorphism in Harmonia axyridis?

dsx regulates color-pattern dimorphism by negatively modulating black spot size in males.

What role does gene h play in dsx-mediated regulation?

The modulation is primarily mediated through transcriptional regulation of the color-patterning gene h.

Sep 29, 2026

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