Precise staging of beetle horn formation in Trypoxylus dichotomus reveals the pleiotropic roles of doublesex depending on the spatiotemporal developmental contexts
Precise staging of beetle horn formation in Trypoxylus dichotomus reveals the pleiotropic roles of doublesex depending on the spatiotemporal developmental contexts
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DOI：
10.1371/journal.pgen.1008063
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发表时间：
2019-04-01
期刊：
影响因子：
4.5
通讯作者：
Niimi, Teruyuki
中科院分区：
文献类型：
--
作者：
Morita, Shinichi;Ando, Toshiya;Niimi, Teruyuki
许多圣甲虫具有两性异形的夸张角，这是进化上的新奇事物。由于金龟子科内角的形状、数量、大小和位置存在很大差异，因此甲虫角是研究两性异形和新特征进化的一个有吸引力的模型。在包括日本犀牛甲虫 Trypoxylus dichotomus 在内的甲虫中，性别分化基因 doublesex (dsx) 在幼虫-蛹发育过程中两性角的形成中起着至关重要的作用。然而，关于 dsx 在发育过程中何时以及如何驱动角形成的基因调控网络 (GRN) 形成性二态性角的知识仍然难以捉摸。为了解决这个问题，我们鉴定了性别决定基因 Transformer (tra) 的 Trypoxylus 直系同源物，它调节 dsx pre-mRNA 的性别特异性剪接，其功能丧失会导致性别转变。通过在幼虫-蛹发育过程中的多个发育时间点敲除 tra 功能，我们估计了驱动角形成的性别特异性 GRN 的起始时间。此外，我们还揭示了dsx在预蛹和蛹发育阶段调节形态发生活动的不同方面，以形成蛹头和胸角原基以及成虫角的适当形态。基于这些发现，我们讨论了角甲虫两性二态性特征生长的进化发育背景。 作者摘要 金龟子科甲虫的头部和胸部有各种类型的角，并且这些角的形状、大小、数量和位置在类群内高度多样化。此外，许多圣甲虫的角是两性二态的。这些进化上新颖的角的获得，以及这些结构多样化的机制是一个有趣的问题。为了解决这个问题，我们重点关注犀牛甲虫 Tripoxylus dichotomus。在这里，我们确定了角原基形态两性二态性出现的确切发育时间点，估计了由双性驱动的两性角形成的发育程序的开始，并揭示了双性在角形成过程中根据特定的时空发育背景调节细胞活动的不同方面。我们的研究提供了有关角甲虫性二态性状进化过程中这些机制的调节变化的见解。
Many scarab beetles have sexually dimorphic exaggerated horns that are an evolutionary novelty. Since the shape, number, size, and location of horns are highly diverged within Scarabaeidae, beetle horns are an attractive model for studying the evolution of sexually dimorphic and novel traits. In beetles including the Japanese rhinoceros beetle Trypoxylus dichotomus, the sex differentiation gene doublesex (dsx) plays a crucial role in sexually dimorphic horn formation during larval-pupal development. However, knowledge of when and how dsx drives the gene regulatory network (GRN) for horn formation to form sexually dimorphic horns during development remains elusive. To address this issue, we identified a Trypoxylus-ortholog of the sex determination gene, transformer (tra), that regulates sex-specific splicing of the dsx pre-mRNA, and whose loss of function results in sex transformation. By knocking down tra function at multiple developmental timepoints during larval-pupal development, we estimated the onset when the sex-specific GRN for horn formation is driven. In addition, we also revealed that dsx regulates different aspects of morphogenetic activities during the prepupal and pupal developmental stages to form appropriate morphologies of pupal head and thoracic horn primordia as well as those of adult horns. Based on these findings, we discuss the evolutionary developmental background of sexually dimorphic trait growth in horned beetles.Author summary Beetles in the family Scarabaeidae have various types of horns on their heads and thoraces, and the shape, size, number, and location of these horns are highly diversified within the group. In addition, many scarab beetle horns are sexually dimorphic. The acquisition of these evolutionarily novel horns, and the mechanisms for the diversification of these structures is an interesting question. To address this question, we focused on the rhinoceros beetle Tripoxylus dichotomus. Here we identified the exact developmental timepoints during which the morphological sexual dimorphism of horn primordia appears, estimated the onset of the developmental program for sexually dimorphic horn formation driven by doublesex, and revealed that doublesex regulates different aspects of cell activities during horn formation depending on particular spatiotemporal developmental contexts. Our study provides insights into regulatory shifts in these mechanisms during the evolution of sexually dimorphic traits in horned beetles.