Perlin Michael H, Poulin Robert, de Bekker Charissa
Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, Kentucky, 40208, USA.
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand.
Biol Rev Camb Philos Soc. 2025 Apr;100(2):936-968. doi: 10.1111/brv.13169. Epub 2024 Dec 1.
Parasites have a rich and long natural history among biological entities, and it has been suggested that parasites are one of the most significant factors in the evolution of their hosts. However, it has been emphasized less frequently how co-evolution has undoubtedly also shaped the paths of parasites. It may seem safe to assume that specific differences among the array of potential hosts for particular parasites have restricted and diversified their evolutionary pathways and strategies for survival. Nevertheless, if one looks closely enough at host and parasite, one finds commonalities, both in terms of host defences and parasite strategies to out-manoeuvre them. While such analyses have been the source of numerous reviews, they are generally limited to interactions between, at most, one kingdom of parasite with two kingdoms of host (e.g. similarities in animal and plant host responses against fungi). With the aim of extending this view, we herein critically evaluate the similarities and differences across all four eukaryotic host kingdoms (plants, animals, fungi, and protists) and their parasites. In doing so, we show that hosts tend to share common strategies for defence, including both physical and behavioural barriers, and highly evolved immune responses, in particular innate immunity. Parasites have, similarly, evolved convergent strategies to counter these defences, including mechanisms of active penetration, and evading the host's innate and/or adaptive immune responses. Moreover, just as hosts have evolved behaviours to avoid parasites, many parasites have adaptations to manipulate host phenotype, physiologically, reproductively, and in terms of behaviour. Many of these strategies overlap in the host and parasite, even across wide phylogenetic expanses. That said, specific differences in host physiology and immune responses often necessitate different adaptations for parasites exploiting fundamentally different hosts. Taken together, this review facilitates hypothesis-driven investigations of parasite-host interactions that transcend the traditional kingdom-based research fields.
在生物实体中，寄生虫拥有丰富而悠久的自然历史，有人认为寄生虫是其宿主进化的最重要因素之一。然而，人们较少强调共同进化无疑也塑造了寄生虫的发展路径。可以设想，特定寄生虫潜在宿主群体之间的特定差异限制并多样化了它们的进化途径和生存策略。然而，如果仔细观察宿主和寄生虫，就会发现它们在宿主防御和寄生虫应对策略方面存在共性。虽然此类分析已成为众多综述的来源，但它们通常最多限于一个寄生虫界与两个宿主界之间的相互作用（例如动植物宿主对真菌反应的相似性）。为了拓展这一观点，我们在此严格评估了所有四个真核宿主界（植物、动物、真菌和原生生物）及其寄生虫之间的异同。通过这样做，我们发现宿主倾向于共享共同的防御策略，包括物理和行为屏障以及高度进化的免疫反应，尤其是先天免疫。同样，寄生虫也进化出了趋同策略来对抗这些防御，包括主动穿透机制以及逃避宿主的先天和/或适应性免疫反应。此外，正如宿主进化出行为来避免寄生虫一样，许多寄生虫也有适应机制来在生理、生殖和行为方面操纵宿主表型。这些策略中的许多在宿主和寄生虫中重叠，甚至跨越广泛的系统发育范围。也就是说，宿主生理和免疫反应的特定差异通常需要寄生虫针对根本不同的宿主进行不同的适应。综上所述，本综述有助于开展以假设为驱动的寄生虫 - 宿主相互作用研究，超越传统的基于界的研究领域。
