NSFDEB-NERC: Integrating phylogenomics, biophysics, and functional genomics to unravel the evolution of hearing and singing in Ensifera (katydids, crickets and relatives)

就像人类用声音彼此交谈一样，许多其他动物也用声音进行交流。利用声音来发送和接收信息，被称为声音通信，在许多不同类型的动物中都有发现，包括昆虫、鸟类、青蛙和哺乳动物。在这些动物中，会唱歌的昆虫，如蟋蟀和蝈蝈，是第一批进化出听觉和发声能力的动物，估计在3亿年前。从那时起，蟋蟀、蝈蝈和它们的亲戚（小蟋蟀）已经广泛多样化，产生了大约15000个已知的物种，以及几种不同的听觉和歌唱机制。它们现在代表了依靠声音交流的最多样化的生物群体。因此，研究这些昆虫的听觉和歌唱是如何进化和多样化的，可以揭示动物交流的起源和进化的重要见解。这项由美国、英国、法国等国科学家参与的合作研究项目将收集大量基因数据，重建蟋蟀、蝈蝈及其近亲之间的进化关系。该团队还将采用三维成像、生物物理学和基因组学方面的尖端技术来研究这些昆虫的听觉和歌唱的不同机制。该项目将填补了解该群体生物多样性和生物声学方面的重要空白，并提供独特的教育机会，包括针对K-12学生的项目外展活动，为六名波利尼西亚和西班牙裔本科生提供实践本科研究经验，以及培训两名研究生和两名博士后研究人员。该项目将根据目标捕获DNA测序产生的1600个物种和1000个位点，生成现存歌唱昆虫中物种最多、最古老的谱系——Ensifera（蟋蟀、蝈蝈儿及其近亲）的综合系统发育日期。利用这种系统发育作为一个强大的比较框架，研究人员将利用x射线微纳米计算机断层扫描、微扫描激光多普勒振动仪和RNA-seq技术，在主要的敏感动物谱系中产生前所未有的详细形态学、生物物理和遗传数据，以确定听觉和歌唱的机制。研究人员将实时测量耳功能，比较听觉器官的三维解剖和生物物理特性，对已灭绝和现存物种的发声器官及其相应的鸣声频率进行大规模的比较分析，生成和比较翅膀脉络基因和胫骨听觉器官转录组。利用这些数据，研究人员将解决几个长期存在的问题，如声音通信何时开始进化以及它丢失的频率，谱系如何独立进化不同的听力和信号机制，这些听力和信号机制的物理，神经和遗传基础是什么，以及信号多样性如何与多样化和物种形成联系在一起。这些发现将共同揭示声音通信进化的一般见解，可以作为研究其他昆虫类似机制的模型。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。

Just as humans use voices to talk to one another, many other animals also use sound for communication. The use of sound to send and receive messages, known as acoustic communication, is found in many different types of animals, including insects, birds, frogs, and mammals. Among these animals, singing insects, such as crickets and katydids, were the first to evolve the ability to hear and produce sound an estimated 300 million years ago. Since then, crickets, katydids, and relatives (Ensifera) have diversified extensively, giving rise to an estimated 15,000 known species, and several different mechanisms of hearing and singing. They now represent the most diverse group of organisms that rely on acoustic communication. Therefore, studying how hearing and singing evolved and diversified in these insects can reveal important insights about the origin and evolution of animal communication. This collaborative research project including scientists from the United States, the United Kingdom, and France will gather a massive amount of genetic data to reconstruct evolutionary relationships among crickets, katydids, and relatives. The team will also employ cutting-edge techniques in three-dimensional imaging, biophysics, and genomics to investigate the diverse mechanisms of hearing and singing in these insects. This project will fill important gaps in understanding the biodiversity and bioacoustics of the group and provide unique educational opportunities including, project-enabled outreach activities targeting K-12 students, hands-on undergraduate research experience to six Polynesian and Hispanic undergraduate students, as well as training of two graduate students and two postdoctoral researchers.This project will produce a comprehensive dated phylogeny of Ensifera (crickets, katydids, and relatives), the most speciose and ancient lineage of the extant singing insects, based on 1,600 species and 1,000 loci generated from target capture DNA sequencing. Using this phylogeny as a robust comparative framework, the researchers will generate an unprecedented amount of detailed morphological, biophysical, and genetic data using X-ray micro- and nano- computed tomography (CT) scanning, micro-scanning laser Doppler vibrometry, and RNA-seq across major ensiferan lineages to identify mechanisms of hearing and singing. Researchers will measure real-time ear function and compare 3-dimensional anatomy and biophysical properties of hearing organs, conduct a large-scale comparative analysis of sound-producing organs and their corresponding song frequencies using both extinct and extant species, and generate and compare wing venation genes and tibial hearing organ transcriptomes. Using these data, researchers will address several longstanding questions about when acoustic communication first evolved and how often it has been lost, how lineages independently evolved different hearing and signaling mechanisms, what the physical, neural and genetic bases of these hearing and signaling mechanisms are, and how signaling diversity is linked to diversification and speciation. These findings will collectively reveal general insights about the evolution of acoustic communication that could serve as a model for the study of similar mechanisms in other insects.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.