Data from: Expression and phylogenetic analyses reveal paralogous lineages of putatively classical and non-classical MHC-I genes in three sparrow species (Passer)

Background: The Major Histocompatibility Complex (MHC) plays a central role in immunity and has been given considerable attention by evolutionary ecologists due to its associations with fitness-related traits. Songbirds have unusually high numbers of MHC class I (MHC-I) genes, but it is not known whether all are expressed and equally important for immune function. Classical MHC-I genes are highly expressed, polymorphic and present peptides to T-cells whereas non-classical MHC-I genes have lower expression, are more monomorphic and do not present peptides to T-cells. To get a better understanding of the highly duplicated MHC genes in songbirds, we studied gene expression in a phylogenetic framework in three species of sparrows (house sparrow, tree sparrow and Spanish sparrow), using high-throughput sequencing. We hypothesize that sparrows could have classical and non-classical genes, as previously indicated though never tested using gene expression.
Results: The phylogenetic analyses reveal two distinct types of MHC-I alleles among the three sparrow species, one with high and one with low level of polymorphism, thus resembling classical and non-classical genes, respectively. All individuals had both types of alleles, but there was copy number variation both within and among the sparrow species. However, the number of highly polymorphic alleles that were expressed did not vary between species, suggesting that the structural genomic variation is counterbalanced by conserved gene expression. Overall, 50% of the MHC-I alleles were expressed in sparrows. Expression of the highly polymorphic alleles was very variable, whereas the alleles with low polymorphism had uniformly low expression. Interestingly, within an individual only one or two alleles from the polymorphic genes were highly expressed, indicating that only a single copy of these is highly expressed.
Conclusions: Taken together, the phylogenetic reconstruction and the analyses of expression suggest that sparrows have both classical and non-classical MHC-I genes, and that the evolutionary origin of these genes predate the split of the three investigated sparrow species seven million years ago. Because only the classical MHC-I genes are involved in antigen presentation, the function of different MHC-I genes should be considered in future ecological and evolutionary studies of MHC-I in sparrows and other songbirds.

背景：主要组织相容性复合体（Major Histocompatibility Complex, MHC）在免疫反应中发挥核心作用，且因其与适应性相关性状存在关联，受到进化生态学家的广泛关注。鸣禽的MHC I类（MHC-I）基因数量异常丰富，但目前尚不清楚所有这类基因是否均会表达，以及它们在免疫功能中是否发挥同等重要的作用。经典MHC-I基因表达量高、多态性丰富，可将肽段呈递给T细胞；而非经典MHC-I基因表达量较低、多态性较低，且无法将肽段呈递给T细胞。为深入解析鸣禽中高度重复的MHC基因，本研究以三种雀形目鸟类（家麻雀、树麻雀和西班牙麻雀）为研究对象，采用高通量测序技术，在系统发育框架下开展基因表达分析。我们提出假设：麻雀类群可能同时存在经典与非经典MHC基因，这一推测此前已被提出，但从未通过基因表达实验得到验证。
结果：系统发育分析显示，三种麻雀的MHC-I等位基因可分为两类截然不同的类型，一类具有较高的多态性，另一类多态性较低，分别对应经典与非经典MHC基因。所有个体均携带两类等位基因，但在物种内部以及物种之间均存在拷贝数变异。不过，表达的高多态性等位基因数量在物种间并无差异，这表明基因组结构变异可通过保守的基因表达水平得以平衡。总体而言，麻雀中50%的MHC-I等位基因得到了表达。高多态性等位基因的表达水平差异极大，而低多态性等位基因则始终保持低水平表达。值得注意的是，单个个体中仅有一种或两种来自多态性基因的等位基因呈现高表达，这说明这类基因仅单拷贝会发生高水平表达。
结论：综合系统发育重建与基因表达分析结果可知，麻雀类群同时存在经典与非经典MHC-I基因，且这类基因的演化起源早于700万年前三种研究对象麻雀的分化事件。由于仅经典MHC-I基因参与抗原呈递，因此在未来针对麻雀及其他鸣禽的MHC-I生态与进化研究中，应当考虑不同MHC-I基因的功能差异。