Evolution of sexually dimorphic pheromone profiles coincides with increased number of male-specific chemosensory organs in Drosophila prolongata

Binary communication systems that involve sex-specific signaling and sex-specific signal perception play a key role in sexual selection and in the evolution of sexually dimorphic traits. The driving forces and genetic changes underlying such traits can be investigated in systems where sex-specific signaling and perception have emerged recently and show evidence of potential coevolution. A promising model is found in Drosophila prolongata, which exhibits a species-specific increase in the number of male chemosensory bristles. We show that this transition coincides with recent evolutionary changes in cuticular hydrocarbon (CHC) profiles. Long-chain CHCs that are sexually monomorphic in the closest relatives of D. prolongata (D. rhopaloa, D. carrolli, D. kurseongensis, and D. fuyamai) are strongly male-biased in this species. We also identify an intraspecific female-limited polymorphism, where some females have male-like CHC profiles. Both the origin of sexually dimorphic CHC profiles and the female-limited polymorphism in D. prolongata involve changes in the relative amounts of three mono-alkene homologs, 9-Tricosene, 9-Pentacosene and 9-Heptacosene, all of which share a common biosynthetic origin and point to a potentially simple genetic change underlying these traits. Our results suggest that pheromone synthesis may have coevolved with chemosensory perception, and open the way for reconstructing the origin of sexual dimorphism in this communication system.

涉及性别特异性信号传导与性别特异性信号感知的二元通信系统，在性选择以及性别二态性性状的演化过程中发挥着关键作用。针对那些新近演化出性别特异性信号传导与感知、且展现出潜在共演化证据的研究体系，我们可以对这类性状背后的驱动因素与遗传变化展开探究。长须果蝇（Drosophila prolongata）便是极具潜力的研究模型：该物种的雄性化学感受刚毛数量存在物种特异性提升。我们的研究表明，这一转变与表皮碳氢化合物（cuticular hydrocarbon, CHC）谱的新近演化变化相契合。在长须果蝇的近缘姊妹物种（D. rhopaloa、D. carrolli、D. kurseongensis与D. fuyamai）中，长链表皮碳氢化合物呈性别单态性，而在该物种中则呈现强烈的雄性偏向性。我们还发现了一种种内雌性限制性多态现象：部分雌性个体拥有类似雄性的表皮碳氢化合物谱。无论是长须果蝇中性别二态性表皮碳氢化合物谱的起源，还是其雌性限制性多态现象，均涉及三类单烯烃同系物相对含量的变化——即9-二十三碳烯（9-Tricosene）、9-二十五碳烯（9-Pentacosene）与9-二十七碳烯（9-Heptacosene），这三类物质拥有共同的生物合成起源，提示这些性状背后可能存在较为简单的遗传变化基础。我们的研究结果表明，信息素合成或许已与化学感应感知协同演化，同时为解析该通信系统中性二态性的起源提供了可行的研究路径。