Patterns of immunogenetic and malarial parasite diversity in three species of Vietnamese passerines

Understanding how genetic diversity in host immune genes affects susceptibility to pathogen infections is crucial for deciphering host-pathogen coevolutionary dynamics. In this study, we investigated the genetic diversity of mitochondrial cytochrome b (cyt b) and key immune genes including Toll-like receptors (TLR3 exon 4 and TLR4 exon 3) and the major histocompatibility complex (MHC class I exon 3) in three sympatric passerine bird species (Arachnothera longirostra, Copsychus malabaricus, and Pitta moluccensis) from Southeast Asia, includinh their associations with Plasmodium infections. Our cyt b analyses indicated that A. longirostra experienced past population expansions, evidenced by significantly low Tajima's D and Fu's Fs values, whereas C. malabaricus and P. moluccensis maintained relatively constant effective population sizes. Immune gene diversity revealed unique profiles across the three species: MHC class I genes displayed positive Tajima's D values, suggesting balancing selection and possible historical bottlenecks, particularly in A. longirostra and P. moluccensis. Selection analyses showed that MHC genes are primarily under purifying selection with species-specific codons under diversifying selection. TLR genes were predominantly governed by purifying selection, with minor instances of diversifying selection noted. Generalized linear models demonstrated that the total number of MHC supertypes did not significantly influence Plasmodium infection status across passerine species, providing no support for the heterozygote advantage hypothesis. However, in P. moluccensis, specific MHC supertypes were significantly associated with Plasmodium operational taxonomic units (OTUs), indicating a possible rare-allele advantage in MHC-mediated malaria resistance. These findings highlight the complex interplay between host genetic diversity and parasite infection, suggesting that balancing selection on immune genes may vary even among sympatric species facing similar pathogen pressures.阐明宿主免疫基因的遗传多样性如何影响病原体感染易感性，对于解析宿主与病原体的协同进化动态至关重要。本研究针对东南亚地区3种同域分布雀形目鸟类——长嘴捕蛛鸟（Arachnothera longirostra）、白腰鹊鸲（Copsychus malabaricus）以及蓝翅八色鸫（Pitta moluccensis），分析了其线粒体细胞色素b（cytochrome b, cyt b）以及Toll样受体（Toll-like receptors, TLR）3外显子4、TLR4外显子3和主要组织相容性复合体I类分子外显子3（major histocompatibility complex class I exon 3, MHC I类外显子3）等关键免疫基因的遗传多样性，并探讨了这些基因与疟原虫（Plasmodium）感染的关联。我们对cyt b的分析结果显示，长嘴捕蛛鸟曾经历过种群扩张，这一结论得到了其极低的Tajima's D和Fu's Fs值的支持；而白腰鹊鸲与蓝翅八色鸫的有效种群大小（effective population size）则相对稳定。免疫基因多样性在3个物种中呈现出独特的模式：MHC I类基因的Tajima's D值为正值，提示存在平衡选择（balancing selection）与潜在的历史瓶颈效应（historical bottlenecks），这一现象在长嘴捕蛛鸟和蓝翅八色鸫中尤为显著。选择压分析结果表明，MHC基因整体处于纯化选择（purifying selection）作用之下，但部分物种特异性密码子位点受到了多样化选择（diversifying selection）的影响。TLR基因则主要受纯化选择主导，仅存在少量多样化选择的案例。广义线性模型（Generalized linear models）分析显示，在所有雀形目物种中，MHC超型（MHC supertypes）的总数并未对疟原虫感染状态产生显著影响，这一结果不支持杂合子优势假说（heterozygote advantage hypothesis）。但在蓝翅八色鸫中，特定的MHC超型与疟原虫操作分类单元（operational taxonomic units, OTUs）存在显著关联，这提示MHC介导的疟疾抗性可能存在稀有等位基因优势（rare-allele advantage）。本研究结果凸显了宿主遗传多样性与寄生虫感染之间复杂的相互作用，表明即使是面临相似病原体压力的同域分布物种，其免疫基因所受的平衡选择作用也可能存在差异。