Drews Anna, Strandh Maria, Råberg Lars, Westerdahl Helena
Department of Biology, Lund University, Ecology Building, 223 62, Lund, Sweden.
BMC Evol Biol. 2017 Jun 26;17(1):152. doi: 10.1186/s12862-017-0970-7.
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.
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.
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 7 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.
主要组织相容性复合体（MHC）在免疫中起核心作用，因其与适应性相关性状的关联而受到进化生态学家的广泛关注。鸣禽拥有数量异常多的MHC I类（MHC-I）基因，但尚不清楚它们是否都有表达以及对免疫功能是否同等重要。经典MHC-I基因高度表达、具有多态性并向T细胞呈递肽段，而非经典MHC-I基因表达水平较低、多态性较低且不向T细胞呈递肽段。为了更好地理解鸣禽中高度重复的MHC基因，我们利用高通量测序技术，在系统发育框架下研究了三种麻雀（家麻雀、树麻雀和西班牙麻雀）的基因表达情况。我们推测麻雀可能拥有经典和非经典基因，正如之前所指出的那样，但从未通过基因表达进行过测试。
系统发育分析揭示了三种麻雀中存在两种不同类型的MHC-I等位基因，一种多态性高，另一种多态性低，分别类似于经典和非经典基因。所有个体都拥有这两种类型的等位基因，但麻雀物种内部和物种之间都存在拷贝数变异。然而，表达的高度多态性等位基因数量在物种间没有差异，这表明结构基因组变异被保守的基因表达所平衡。总体而言，50%的MHC-I等位基因在麻雀中表达。高度多态性等位基因的表达非常多变，而多态性低的等位基因表达一直很低。有趣的是，在一个个体中，多态性基因中只有一两个等位基因高度表达，这表明这些基因中只有一个拷贝高度表达。
综合来看，系统发育重建和表达分析表明麻雀拥有经典和非经典MHC-I基因，并且这些基因的进化起源早于700万年前所研究的三种麻雀物种的分化。由于只有经典MHC-I基因参与抗原呈递，在未来对麻雀和其他鸣禽MHC-I的生态和进化研究中应考虑不同MHC-I基因的功能。
