Adaptive Divergence of Ancient Gene Duplicates in the Avian MHC Class II β

Adaptive Divergence of Ancient Gene Duplicates in the Avian MHC Class II β
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DOI:
10.1093/molbev/msq120
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发表时间:
2010-10-01
影响因子:
10.7
通讯作者:
Fumagalli, Luca
Fumagalli, Luca
中科院分区:
生物学1区
文献类型:
--
作者:
Burri, Reto;Salamin, Nicolas;Fumagalli, Luca

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基因复制和新功能化是表型复杂性进化中的重要过程。它们解释了赋予生态适应的重要进化新颖性,例如主要组织相容性复合体(MHC),一个对脊椎动物免疫系统至关重要的多基因家族。在鸟类中,最近已经鉴定了两个MHCⅡ类β(MHCIIβ)外显子3谱系,并提出了关于MHCIIβ谱系进化史的两个假说。这些谱系可能是由以下两种方式产生的:1)一个并列基因的远古复制和随后的分化,或者2)最近的并行复制和功能趋同。在这里,我们编辑了一个由来自六个鸟类目的63个MHCIIβ外显子3序列组成的数据集,以区分这些假说,并了解选择在两个禽类MHCIIβ谱系分化进化中的作用。基于系统发育重建和模拟,我们表明,在主要鸟类辐射之前发生的独特重复事件导致了两个祖先MHCIIβ谱系的产生,每个谱系都可能在鸟类进化过程中后来丢失一次。最大似然估计表明,在祖先复制之后,正选择导致MHCIIα-β-异二聚体中面向α链的蛋白质结构域的碱性氨基酸组成发生了根本性的转变。对MHCIIα-β-异二聚体的结构分析强调,其中三个残基可能参与与阿尔法链的直接相互作用,这表明复制后的转变可能伴随着相互作用的α-链和β-链的共同进化。这些结果为鸟类MHC基因之间的长期进化关系提供了新的见解,并为鸟类MHC进化的比较和种群基因组研究开辟了有趣的前景。
Gene duplication and neofunctionalization are known to be important processes in the evolution of phenotypic complexity. They account for important evolutionary novelties that confer ecological adaptation, such as the major histocompatibility complex (MHC), a multigene family crucial to the vertebrate immune system. In birds, two MHC class II beta (MHCII beta) exon 3 lineages have been recently characterized, and two hypotheses for the evolutionary history of MHCII beta lineages were proposed. These lineages could have arisen either by 1) an ancient duplication and subsequent divergence of one paralog or by 2) recent parallel duplications followed by functional convergence. Here, we compiled a data set consisting of 63 MHCII beta exon 3 sequences from six avian orders to distinguish between these hypotheses and to understand the role of selection in the divergent evolution of the two avian MHCII beta lineages. Based on phylogenetic reconstructions and simulations, we show that a unique duplication event preceding the major avian radiations gave rise to two ancestral MHCII beta lineages that were each likely lost once later during avian evolution. Maximum likelihood estimation shows that following the ancestral duplication, positive selection drove a radical shift from basic to acidic amino acid composition of a protein domain facing the alpha-chain in the MHCII alpha beta-heterodimer. Structural analyses of the MHCII alpha beta-heterodimer highlight that three of these residues are potentially involved in direct interactions with the alpha-chain, suggesting that the shift following duplication may have been accompanied by coevolution of the interacting alpha- and beta-chains. These results provide new insights into the long-term evolutionary relationships among avian MHC genes and open interesting perspectives for comparative and population genomic studies of avian MHC evolution.