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.
地球上的生物表现出各种形式的两性二态性,包括装饰物、武器特征和信息素腺体,这些都是在进化过程中通过性选择获得的。尽管已经在不同物种中研究了性特征的遗传基础,但在一个物种内两性二态性的获得或丧失过程中,潜在的调节系统是如何进化的,仍然知之甚少。为了解决这一问题,我们研究了异色瓢虫(harlequin ladybug, Harmonia axyridis, H. axyridis)鞘翅颜色模式的品系特异性性别二态性。最基本的红点型颜色形态表现出性别二态性,而其他衍生的颜色形态则失去了它。为了研究这种两性二态性是如何在新颜色形态的进化过程中消失的,我们研究了两性二态性的遗传基础,重点研究了两性分化的主要基因——双性(dsx)。我们发现dsx通过负向调节雄性黑斑大小来调节颜色模式二态性。这种调节主要是由颜色模式基因h (Drosophila pannier ortholog)的转录调节介导的。蛹翅的种内比较ATAC-seq分析显示,在h位点,失去性别二型性并获得新颜色图案的菌株中,含有dsx结合基序的开放染色质区域相对于缺乏这些基序的开放染色质区域的比例减少,而不是dsx结合基序的绝对数量减少,这表明性别二型性的进化是基于新的ccres和dsx结合基序密度之间的平衡。本研究提供了一个基本的分子框架,以了解在水蛭中第二性征是如何进化的。
{"title":"Sex-Specific doublesex Regulation Targeting the Color-Patterning Gene h Underlies the Evolution of Wing Sexual Dimorphism in the Harlequin Ladybug Harmonia axyridis","authors":"Soichi Yeki, Kagayaki Kato, Shinichi Morita, Kenji Shimomura, Teruyuki Niimi, Norihide Hinomoto, Takaaki Daimon, Toshiya Ando","doi":"10.1111/ede.70028","DOIUrl":"https://doi.org/10.1111/ede.70028","url":null,"abstract":"<p>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, <i>Harmonia axyridis</i> (<i>H. axyridis</i>), 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, <i>doublesex</i> (<i>dsx</i>). We show that <i>dsx</i> 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, <i>h</i> (<i>Drosophila pannier</i> ortholog). Intraspecific comparative ATAC-seq analysis of the pupal wings revealed that, at the <i>h</i> 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 <i>H. axyridis</i>.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"28 1","pages":""},"PeriodicalIF":2.6,"publicationDate":"2026-01-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.70028","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145909349","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}