Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, 510260, China.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.
Gigascience. 2024 Jan 2;13. doi: 10.1093/gigascience/giae044.
Sex role differentiation is a widespread phenomenon. Sex pheromones are often associated with sex roles and convey sex-specific information. In Lepidoptera, females release sex pheromones to attract males, which evolve sophisticated olfactory structures to relay pheromone signals. However, in some primitive moths, sex role differentiation becomes diverged. Here, we introduce the chromosome-level genome assembly from ancestral Himalaya ghost moths, revealing a unique olfactory evolution pattern and sex role parity among Lepidoptera. These olfactory structures of the ghost moths are characterized by a dense population of trichoid sensilla, both larger male and female antennal entry parts of brains, compared to the evolutionary later Lepidoptera. Furthermore, a unique tandem of 34 odorant receptor 19 homologs in Thitarodes xiaojinensis (TxiaOr19) has been identified, which presents overlapped motifs with pheromone receptors (PRs). Interestingly, the expanded TxiaOr19 was predicted to have unconventional tuning patterns compared to canonical PRs, with nonsexual dimorphic olfactory neuropils discovered, which contributes to the observed equal sex roles in Thitarodes adults. Additionally, transposable element activity bursts have provided traceable loci landscapes where parallel diversifications occurred between TxiaOr19 and PRs, indicating that the Or19 homolog expansions were diversified to PRs during evolution and thus established the classic sex roles in higher moths. This study elucidates an olfactory prototype of intermediate sex communication from Himalaya ghost moths.
性别角色分化是一种广泛存在的现象。性信息素通常与性别角色相关联，并传递特定于性别的信息。在鳞翅目昆虫中，雌性释放性信息素来吸引雄性，而雄性则进化出复杂的嗅觉结构来传递信息素信号。然而，在一些原始的飞蛾中，性别角色分化变得不同。在这里，我们介绍了来自喜马拉雅幽灵飞蛾的染色体水平基因组组装，揭示了鳞翅目昆虫中独特的嗅觉进化模式和性别角色均等性。与进化后期的鳞翅目昆虫相比，幽灵飞蛾的这些嗅觉结构的特征是密集的毛形感觉器官，以及雄性和雌性触角进入大脑的部分更大。此外，在小金秀眉（TxiaOr19）中鉴定出了一个独特的 34 个气味受体 19 同源物的串联体，它与信息素受体（PRs）具有重叠的基序。有趣的是，与经典的 PRs 相比，扩展的 TxiaOr19 被预测具有非常规的调谐模式，并且发现了非性二态性的嗅觉神经节，这有助于解释在小金秀眉成虫中观察到的平等性别角色。此外，转座元件的活性爆发提供了可追踪的基因座景观，其中 TxiaOr19 和 PRs 之间发生了平行多样化，表明 Or19 同源物的扩展在进化过程中多样化为 PRs，从而在高等飞蛾中建立了经典的性别角色。这项研究阐明了来自喜马拉雅幽灵飞蛾的中间性别通讯的嗅觉原型。
