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。我们的研究将使用一个正在经历极快速进化的备受瞩目的野生昆虫系统来测试关于这种相互依赖的共同进化的基因组基础的假说：野外蟋蟀受到窃听的内寄生蜂苍蝇的致命攻击。当寄主物种的防御性适应驱动其天敌的反适应进化时，共同进化发生，这反过来又发挥有利于宿主适应的选择。理论预测，这种来回可以通过两种常见的模式发生：在军备竞赛(AR)的共同进化中，新的宿主和寄生虫的适应和反适应通过选择性的扫荡进化。这个模型预测寄主和寄生蜂的基因组应该表现出正选择和反复的选择性扫描的特征。相比之下，红皇后(RQ)的模型预测了一场正在进行的拔河比赛，无论是宿主还是寄生虫都不会“获胜”。该模型预测寄主适应和寄生反适应应通过平衡选择保持在多态状态。我们将利用这些模型做出的关于基因组选择的明确预测，在板球/苍蝇系统中测试它们，板球/苍蝇系统是自然界快速适应进化的教科书样本。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这个系统中的共同进化适应，涉及哪些基因组热点，以及对它们的功能的洞察。我们将在两个背景下研究这一点。我们的项目重点关注夏威夷和北美的苍蝇和板球种群。苍蝇幼虫会致命地吞噬寄主，对蟋蟀进行精心研究的选择：在夏威夷，雄性蟋蟀反复进化出失去歌声的适应能力，消除产生声音的翅膀结构，保护它们免受苍蝇的伤害。这些寄主适应给苍蝇施加压力，让它们使用其他感官方式寻找沉默的蟋蟀。相比之下，北美苍蝇攻击不同的宿主物种，这些宿主物种没有进化出雄性沉默适应，但有不同的雄性广告歌曲，苍蝇在当地适应。这种设置提供了一个无与伦比的机会来测试苍蝇对宿主防御的反适应基础上的经典共同进化模型(夏威夷)和苍蝇对宿主信号变化的局部适应(北美)。我们的项目将测量AR和RQ在驱动寄生虫反适应宿主防御方面的证据，允许两者同时运行。我们将通过在苍蝇基因组中划分AR和RQ动态并将它们与功能信息相关联来提供进一步的进展，我们将研究当寄生虫仅限于一个寄主物种与适应多个寄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检查免疫适应以外的特征的共同进化动力学，这在历史上一直是遗传方法的重点，我们的研究还将为昆虫模型提供尖端基因组学资源，用于声接收和听力纳米技术的应用、生物启发的研究。

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.