Collaborative Research: Molecular and evolutionary mechanisms underlying the rapid gain and loss of an insect pheromone

昆虫根据对信息素的感知做出关于繁殖和生存的关键决定，信息素是同一物种成员之间交换的特殊化学信号，表明个体是雄性还是雌性以及其交配状态。在关系密切的物种之间，信息素的化学结构可能不同，这意味着进化速度很快。然而，与翅膀图案等视觉信号或求偶歌曲等听觉信号不同，人们对新的化学信号是如何产生和多样化的知之甚少。该合作项目将研究果蝇产生的抗春药信息素进化的遗传和生化过程。这些发现将加深我们对化学和分子水平的进化如何导致社会行为（如配偶选择）的有机体尺度变化的理解。该研究成果将直接应用于设计基于信息素的策略，以破坏传播疾病的农业害虫和昆虫的繁殖。通过实验室和文献研究经验，将为来自代表性不足的少数民族背景的本科生提供培训机会。与夏威夷语学者合作，学生将通过研究和翻译记录当地昆虫、它们的栖息地和它们在夏威夷文化中的作用的档案材料，从夏威夷土著的角度调查夏威夷昆虫学的历史。这项工作将通过夏威夷马诺阿大学和密歇根州立大学这两个参与机构之间的交流以及当地的公共宣传活动来传播。昆虫占世界物种的80%，它们使用各种各样的化学感觉信号来做出有关繁殖和生存的关键决定。然而，对形成化学感觉特征多样化的生化和遗传过程知之甚少。这个项目的总体目标是了解信息素是如何产生和进化的。该研究将确定控制CH503合成和进化的代谢和遗传机制，CH503是一种在射精球中产生的雄性抗春药信息素，存在于某些种类的果蝇中，但不存在于其他物种中。核心假设是脂质信息素CH503的进化是由次生代谢物的多样化和脂质生物合成基因的组织特异性激活变化驱动的。为了揭示这种信息素快速进化的机制，质谱分析、转录组分析和遗传操作将被用于：1)识别和追踪ch503产生和非产生的射精球代谢组的进化，包括D. melanogaster、同一亚群的其他6个成员和两个远亲物种；2)鉴定和追踪CH503生物合成遗传成分的进化；3)确定将新的生物合成途径引入不产生CH503的物种如何改变射精球的化学特征。将开发的基于高灵敏度质谱的脂质分析方法，以及生成的代谢组学数据，将提供给其他研究人员。该奖项还将有助于培养至少两名博士后学者和六名本科生研究人员，其成果在农业方面具有潜在的应用前景，可用于开发控制昆虫种群的方法。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Insects make critical decisions about reproduction and survival based on the perception of pheromones, specialized chemical signals exchanged between members of the same species that indicate whether an individual is male or female and its mating status. The chemical structures of pheromones can differ between closely related species, implying rapid evolution. However, unlike visual signals like wing patterns or auditory signals like mating songs, little is known about how new chemical signals arise and diversify. This collaborative project will investigate the genetic and biochemical processes that underlie the evolution of an anti-aphrodisiac pheromone produced by Drosophila fruit fly species. The findings will deepen our understanding of how evolution at the chemical and molecular level can lead to organismal-scale changes in social behaviors such as mate choice. The research outcomes will have direct application to the design of pheromone-based strategies to disrupt the reproduction of agricultural pests and insects that transmit disease. Training opportunities will be provided to undergraduate students from underrepresented minority backgrounds through laboratory- and literature-based research experiences. In collaboration with Hawaiian language scholars, students will investigate the history of entomological science in Hawai‘i from a Native Hawaiian perspective by researching and translating archival materials that document endemic insects, their habitats, and their role in Hawaiian culture. That work will be disseminated through exchanges between the two participating institutions, University of Hawai‘i Manoa and Michigan State University, and at local public outreach events. Insects represent 80% of the world’s species and use a wide variety of chemosensory signals to make critical decisions about reproduction and survival. However, little is known about the biochemical and genetic processes that shape the diversification of chemosensory traits. The overall goal of this project is to understand how pheromones originate and evolve. The study will identify the metabolic and genetic mechanisms that control the synthesis and evolution of CH503, a male anti-aphrodisiac pheromone produced in the ejaculatory bulb, which is present in some species of Drosophila, but not others. The central hypothesis is that the evolution of the lipid pheromone CH503 is driven by diversification of secondary metabolites and changes in the tissue-specific activation of lipid biosynthesis genes. To uncover mechanisms underlying the rapid evolution of this pheromone, mass spectrometry, transcriptomic analysis, and genetic manipulation will be used to: 1) identify and trace the evolution of the metabolome of the ejaculatory bulb in CH503-producers and non-producers, including D. melanogaster, six other members of the same subgroup, and two distantly related species; 2) identify and trace the evolution of the genetic components underlying the biosynthesis of CH503; and 3) determine how introduction of a novel biosynthetic pathway to species that do not produce CH503 changes the chemical profile of the ejaculatory bulb. The high-sensitivity mass spectrometry-based methods for lipid analysis to be developed, as well as the metabolomic data generated, will be made available to other researchers. This award will also contribute to the training of at least two post-doctoral scholars and six undergraduate researchers, and the results have potential applications in agriculture for the development of methods to control insect populations.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.