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

就像人类使用声音相互交谈一样，许多其他动物也使用声音进行交流。利用声音发送和接收信息，称为声学交流，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，如蟋蟀和麒麟，在大约3亿年前最先进化出听到和发出声音的能力。从那时起，蟋蟀、katydids和近亲(Ensifera)已经广泛地多样化，产生了大约15,000个已知物种，以及几种不同的听力和歌唱机制。它们现在代表了依赖声音通信的最多样化的有机体群体。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。这个包括美国、英国和法国科学家在内的合作研究项目将收集大量的基因数据，以重建蟋蟀、浣熊和近亲之间的进化关系。该团队还将利用三维成像、生物物理学和基因组学中的尖端技术来研究这些昆虫的听觉和歌唱的不同机制。这个项目将填补在了解该群体的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学生的项目支持的外展活动，为6名波利尼西亚和西班牙裔本科生提供的实践本科研究经验，以及对2名研究生和2名博士后研究人员的培训。该项目将根据目标捕获DNA测序产生的1,600个物种和1,000个基因座，产生一个全面的Ensifera(蟋蟀、麒麟和近亲)的年代系统学。利用这一系统发育作为一个强大的比较框架，研究人员将利用X射线微纳计算机断层扫描(CT)、微扫描激光多普勒测振仪和RNA-SEQ技术生成前所未有的大量详细的形态、生物物理和遗传学数据，以确定听力和歌唱的机制。研究人员将实时测量耳朵功能，比较听力器官的三维解剖和生物物理特性，使用灭绝和现存物种对发声器官及其对应的歌曲频率进行大规模比较分析，并生成和比较翅膀脉络基因和胫骨听力器官转录本。利用这些数据，研究人员将解决几个长期存在的问题，这些问题包括：声音通信最初是在什么时候进化的，消失的频率是多少；谱系是如何独立进化出不同的听力和信号机制的；这些听力和信号机制的物理、神经和遗传基础是什么；信号多样性与多样性和物种形成是如何联系在一起的。这些发现将共同揭示关于声学通信进化的一般见解，可以作为研究其他昆虫中类似机制的模型。这一奖项反映了NSF的法定使命，并通过使用基金会的智力优势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.