Minias Piotr, Peng Wei-Xuan V-H, Matson Kevin D
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237, Łódź, Poland.
Wildlife Ecology and Conservation Group, Wageningen University & Research, Droevendaalsesteeg 3a, 6708PB, Wageningen, Netherlands.
Front Zool. 2023 Sep 8;20(1):32. doi: 10.1186/s12983-023-00511-1.
The development, maintenance, and use of immune defences are costly. Therefore, animals face trade-offs in terms of resource allocation within their immune system and between their immune system and other physiological processes. To maximize fitness, evolution may favour investment in one immunological defence or subsystem over another in a way that matches a species broader life history strategy. Here, we used phylogenetically-informed comparative analyses to test for relationships between two immunological components. Natural antibodies and complement were used as proxies for the innate branch; structural complexity of the major histocompatibility complex (MHC) region was used for the acquired branch.
We found a negative association between the levels of natural antibodies (i.e., haemagglutination titre) and the total MHC gene copy number across the avian phylogeny, both at the species and family level. The family-level analysis indicated that this association was apparent for both MHC-I and MHC-II, when copy numbers within these two MHC regions were analysed separately. The association remained significant after controlling for basic life history components and for ecological traits commonly linked to pathogen exposure.
Our results provide the first phylogenetically robust evidence for an evolutionary trade-off within the avian immune system, with a more developed acquired immune system (i.e., more complex MHC architecture) in more derived bird lineages (e.g., passerines) being accompanied by an apparent downregulation of the innate immune system.
免疫防御的发育、维持和使用成本高昂。因此，动物在免疫系统内以及免疫系统与其他生理过程之间的资源分配方面面临权衡。为了使适应性最大化，进化可能会以一种与物种更广泛的生活史策略相匹配的方式，倾向于对一种免疫防御或子系统而非另一种进行投资。在此，我们使用系统发育信息比较分析来检验两种免疫成分之间的关系。天然抗体和补体被用作先天免疫分支的代表；主要组织相容性复合体（MHC）区域的结构复杂性被用于获得性免疫分支。
我们发现，在鸟类系统发育中，无论是在物种水平还是科水平上，天然抗体水平（即血凝滴度）与MHC基因总拷贝数之间均呈负相关。科级分析表明，当分别分析这两个MHC区域内的拷贝数时，这种关联在MHC-I和MHC-II中均很明显。在控制了基本生活史成分和通常与病原体暴露相关的生态特征后，这种关联仍然显著。
我们的结果首次提供了系统发育上可靠的证据，证明鸟类免疫系统内存在进化权衡，在进化程度更高的鸟类谱系（如雀形目鸟类）中，获得性免疫系统更发达（即MHC结构更复杂），同时先天免疫系统明显下调。
