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

宿主-寄生虫协同进化的基因组学：野生昆虫系统中军备竞赛和红皇后动力学的测试

• 批准号: NE/W001616/1
• 负责人: Nathan Bailey
• 金额: $ 50.38万
• 依托单位: University of St Andrews
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2022
• 资助国家: 英国
• 起止时间: 2022 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FW001616%2F1
• 关键词: Genomics; Host; Parasite; Coevolution; Test

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.

寄生虫和它们的宿主一起进化。我们的研究将测试假设的基因组基础上，这种相互依赖的共同进化使用一个高调的，野生昆虫系统经历了非常迅速的进化：场蟋蟀是致命的攻击，由窃听endoparasitoid苍蝇，Ormia ochracea.Coevolution发生时，宿主物种的防御性适应驱动的进化，在其天敌的反适应，这反过来又发挥选择有利于主机适应。理论预测，这种来回可以通过两种一般模式发生：在军备竞赛（AR）共同进化中，新的宿主和寄生虫适应和反适应通过选择性扫描进化。该模型预测，主机和寄生蜂的基因组应显示积极的选择和经常性的选择性扫描的签名。相比之下，红皇后（RQ）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，宿主适应和寄生虫counteradaptations应保持在一个多态性的状态，通过平衡选择。我们将利用这些模型对基因组选择的明确预测，在蟋蟀/苍蝇系统中测试它们，这是自然界快速适应性进化的教科书范例。我们将使用人口基因组学的方法与尖端的全基因组重测序数据来测试一系列的假设，将揭示是否一个，另一个，或两种模式的共同进化解释共同进化的适应在这个系统中，什么基因组的“热点”参与，并深入了解他们的功能。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。苍蝇幼虫会致命地吞噬宿主，对蟋蟀施加研究充分的选择：在夏威夷，雄性蟋蟀反复进化出失去鸣叫的适应性，抹去产生声音的翅膀结构，保护它们免受苍蝇的伤害。这些宿主的适应性对苍蝇施加压力，迫使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，没有进化出男性沉默的适应，但有不同的男性广告歌曲，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经典的共同进化模型的基础飞反适应主机防御（夏威夷）和飞本地适应主机信号的变化（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，使两者可以同时运作。我们将提供进一步的进展，分区AR和RQ动力学在苍蝇基因组，并将它们与功能信息，我们将研究共同进化的遗传基础时，寄生虫是有限的一个宿主物种与适应多个宿主物种。一个主要的好处是我们计划研究超越免疫适应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，我们的研究还将为应用于生物的昆虫模型提供尖端的基因组学资源。

项目成果

Social Plasticity Enhances Signal-Preference Codivergence

• DOI: 10.1086/726786
• 发表时间: 2023-12-01
• 期刊: AMERICAN NATURALIST
• 影响因子: 2.9
• 作者: Desjonqueres，Camille;Speck，Bretta;Rodriguez，Rafael L.
• 通讯作者: Rodriguez，Rafael L.

Rapid sexual signal diversification is facilitated by permissive females

• DOI: 10.1016/j.cub.2023.11.063
• 发表时间: 2024-01-22
• 期刊: CURRENT BIOLOGY
• 影响因子: 9.2
• 作者: Zhang，Renjie;Rayner，Jack G.;Bailey，Nathan W.
• 通讯作者: Bailey，Nathan W.