Host-parasite coadaptation in a warming world

全球变化正在加剧升温事件和疾病暴发的频率和严重程度。然而，热应激和感染对物种进化和持久性的影响程度尚不清楚。通过造成压力和破坏体内平衡，寄生虫感染可能会破坏宿主应对极端环境的能力。环境科学面临的一个关键挑战是要足够详细地了解这双重威胁之间的相互作用，以预测物种未来将如何应对。因此，考虑温度应激和动物感染的影响对于在与政策相关的时间尺度上管理自然系统至关重要。本项目将在一个微观的线虫-微生物寄生虫相互作用中解决这个问题。这些是全球发现的动植物微生物群的成员，但最初是在腐烂的香蕉茎上分离出来的。考虑到它们短暂的世代时间和相互作用带来的适应性结果，这些物种有可能在数周内迅速共同进化，以应对实验室和自然栖息地的极端温度。然而，由于在自然系统中追踪共同进化的挑战，在变暖期间野生宿主-寄生虫群落的典型共同进化速度在很大程度上仍然未知。我们将利用自然收集、测序、选择实验和模型秀丽隐杆线虫的可处理能力，来记录宿主-寄生虫在变暖情景下共同进化的模式和潜在过程。我们之前已经在实验室中开发了该系统的实验进化，并且其他人已经对其在该领域的多样性进行了分析。在这里，我们将整合这些方法并量化共同进化动力学及其对宿主热性能的影响。首先，我们将在佛得角和加那利群岛的香蕉种植园中共同隔离线虫和寄生虫。我们将量化宿主和寄生虫的热性能。我们将研究在感染期间是否存在不同海拔的热性能差异-目前在野生传染病系统中尚不清楚。这项工作将阐明宿主-寄生虫相互作用对物种在全球分布中生存热应激能力的重要性。其次，我们将在一个进化实验中共同传代线虫和寄生虫种群，其中变暖制度将被操纵。共同适应测试将确定宿主和寄生虫是否在局部斑块内共同进化，然后评估共同适应对中宿主的热极限和寄生虫的毒力。此外，测序将确定宿主是否在基因组成和基因表达方面在变暖机制中存在差异。最后，我们将通过跟踪宿主耐药性和寄生虫传染性随时间的变化来描述共同进化的速度。我们将使用性能分析和基因组学来测试变暖是否会破坏或加速共同进化的相互作用，热浪有利于寄生虫不成比例地更快地适应，而逐渐变暖使宿主有时间在共同进化的竞争中“赶上”。这项工作将产生一种在极端环境下建立共同进化速率和稳定性的新方法-可用于其他微生物和传染病系统。

Global changes are escalating the frequency and severity of heating events and disease outbreaks. The extent to which thermal stress and infection may impact species evolution and persistence is however unclear. By causing stress and disrupting homeostasis, parasite infection may disrupt a host's ability to cope with extreme environments. A key challenge for environmental science is to understand the interaction between these dual threats in enough detail to predict how species will respond in the future. Accounting for the impact of both temperature stress and infection in animals is therefore vital for managing natural systems over policy-relevant timescales. This project will tackle this problem in a microscopic Caenorhabditis nematode-microbial parasite interaction. These are members of animal and plant microbiota found globally, but originally isolated together on rotting banana stems. Given their short generation times and the fitness consequences of their interaction, these species have the potential to coevolve rapidly over weeks and in response to extreme temperatures, in the lab and in their natural habitat. The typical speed of coevolution in wild host-parasite communities during warming remains largely unknown, however, due to challenges in tracking coevolution in natural systems. We will take advantage of natural collections, sequencing, selection experiments, and the tractable power of the model C. elegans, to document patterns and potential processes of host-parasite coevolution across warming scenarios. We have previously developed experimental evolution for this system in the laboratory and its diversity in the field has been assayed by others. Here, we will integrate these approaches and quantify coevolutionary dynamics and its impact on host thermal performance. Firstly, we will co-isolating nematodes and parasites across banana plantations in Cape Verde and Canary Islands. We will quantify host and parasite thermal performances. We will examine whether there is divergence across altitudes in thermal performance during infection - currently unknown in wild infectious disease systems. This work will shed light on the importance of host-parasite interactions on a species' ability to survive thermal stress across its global distribution. Secondly, we will co-passage nematode and parasite populations in an evolution experiment in which warming regimes will be manipulated. Tests for co-adaptation will determine whether hosts and parasite coevolved locally within patches, followed by an assessment of a host's thermal limits and parasite virulence in co-adapted pairs. Further, sequencing will determine whether hosts have diverged in genetic composition and gene expression across warming regimes. Lastly, we will characterise the tempo of coevolution by tracking changes over time in host resistance and parasite infectivity. We will use performance assays and genomices to test whether warming can break down or accelerate coevolutionary interactions, with heat waves favouring disproportionately faster parasite adaptation but gradual warming giving hosts time to 'catch up' in the coevolutionary race. This work will yield a new way to establish coevolutionary rate and stability in the face of extreme environments - usable in other microbial and infectious disease systems.