Genomics of Host-Parasite Coevolution: A Test of Arms Race and Red Queen Dynamics in a Wild Insect System

寄生虫和它们的宿主一起进化。我们的研究将测试关于这种相互依赖的共同进化的基因组基础的假设，使用一个备受瞩目的、正在经历极其快速进化的野生昆虫系统：被窃听的类内寄生蝇Ormia ochracea致命攻击的蟋蟀。当宿主物种的防御性适应驱动其天敌的反适应进化时，共同进化就发生了，而反适应进化反过来又产生了有利于宿主适应的选择。理论预测这种反反复复可以通过两种一般模式发生：在军备竞赛（AR）共同进化中，新宿主和寄生虫的适应和反适应通过选择性清除进化。该模型预测寄主和拟寄生虫基因组应该显示出正选择和周期性选择性扫描的特征。相比之下，红皇后（RQ）模型预测了一场持续的拔河，宿主和寄生虫都不会“赢”。该模型预测寄主的适应和寄主的反适应应通过平衡选择维持在多态状态。我们将利用这些模型对基因组选择做出的明确预测，在蟋蟀/苍蝇系统中进行测试，这是自然界快速适应性进化的教科书范例。我们将使用种群基因组学方法和尖端的全基因组重测序数据来测试一系列假设，这些假设将揭示共同进化的一种，另一种或两种模式是否解释了该系统中的共同进化适应，涉及哪些基因组“热点”，以及对其功能的洞察。我们将在两个上下文中对此进行研究。我们的项目集中在夏威夷和北美的苍蝇和蟋蟀种群。苍蝇幼虫致命地吞噬宿主，对蟋蟀进行了充分研究的选择：在夏威夷，雄性蟋蟀不断进化出丧失歌声的适应能力，抹去发出声音的翅膀结构，保护它们免受苍蝇的伤害。这些寄主的适应性对果蝇施加压力，迫使它们利用其他感官方式寻找沉默的蟋蟀。相比之下，北美蝇攻击不同的寄主物种，这些寄主物种没有进化出雄性沉默的适应能力，但它们有不同的雄性广告歌，这些苍蝇在当地已经适应了。这种设置提供了一个无与伦比的机会来测试经典的共同进化模型，这些模型揭示了苍蝇对宿主防御的反适应（夏威夷）和苍蝇对宿主信号变化的局部适应（北美）。我们的项目将评估AR和RQ在驱动寄生虫对抗宿主防御方面的证据，允许两者同时起作用。我们将在果蝇基因组中划分AR和RQ动态，并将其与功能信息联系起来，从而提供进一步的进展。我们将研究寄生虫局限于一种宿主物种与适应多种宿主物种时共同进化的共同遗传基础。一个主要的好处是，我们计划研究免疫适应以外的性状的共同进化动力学，这在历史上一直是遗传方法的重点，我们的研究还将为用于声学接收和听觉纳米技术应用的生物启发研究的昆虫模型提供尖端的基因组学资源。

Parasites and their hosts evolve together. Our research will test hypotheses about the genomic basis of this mutually-dependent coevolution using a high-profile, wild insect system undergoing extremely rapid evolution: field crickets that are fatally attacked by an eavesdropping endoparasitoid fly, Ormia ochracea.Coevolution occurs when defensive adaptations of a host species drive the evolution of counter-adaptation in their natural enemies, which in turn exerts selection favouring host adaptation. Theory predicts that this back-and-forth can occur via two general modes: in arms race (AR) coevolution, new host and parasite adaptations and counteradaptations evolve via selective sweeps. This model predicts that host and parasitoid genomes should show signatures of positive selection and recurrent selective sweeps. In contrast, Red Queen (RQ) models predict an ongoing tug-of-war which neither host nor parasite ever "wins". This model predicts that host adaptations and parasite counteradaptations should be maintained in a polymorphic state by balancing selection. We will take advantage of the clear predictions about genomic selection that these models make to test them in the cricket/fly system, a textbook exemplar for rapid adaptive evolution in nature. We will use a population genomics approach with cutting-edge whole genome resequencing data to test a series of hypotheses that will reveal whether one, the other, or both modes of coevolution explain coevolutionary adaptation in this system, what genomic 'hotspots' are involved, and insight into their function. We will examine this in two contexts. Our project focuses on fly and cricket populations in Hawaii and North America. Fly larvae fatally consume hosts, exerting well-studied selection on the crickets: in Hawaii, males repeatedly evolved song-loss adaptations that erase sound-producing wing structures, protecting them from flies. These host adaptations exert pressure on the flies to find silent crickets using other sensory modalities. In contrast, North American flies attack different host species which have not evolved male-silencing adaptations, yet have different male advertisement songs to which the flies are locally adapted. This set-up provides an unparalleled opportunity to test classic coevolutionary models underlying fly counter-adaptation to host defences (Hawaii) and fly local adaptation to host signal variation (North America). Our project will gauge evidence for AR and RQ in driving parasite counter-adaptations to host defenses, allowing that both might operate simultaneously. We will provide further advances by partitioning AR and RQ dynamics across the fly genome and relate them to functional information, and we will examine shared genetic bases of coevolution when a parasite is limited to one host species versus adaptation to multiple host species. A major benefit is our plan to examine coevolutionary dynamics of traits beyond immunological adaptations, which have historically been a focus of genetic approaches, and our research will also provide cutting-edge genomics resources for an insect model used in applied, bio-inspired research on nanotechnology of acoustic reception and hearing.