Data from: Lack of evidence for selection favouring MHC haplotypes that combine high functional diversity

High rates of gene duplication and the highest levels of functional allelic diversity in vertebrate genomes are the main hallmarks of the major histocompatibility complex (MHC), a multigene family with a primordial role in pathogen recognition. The usual tight linkage among MHC gene duplicates may provide an opportunity for the evolution of haplotypes that associate functionally divergent alleles and thus grant the transmission of optimal levels of diversity to coming generations. Even though such associations may be a crucial component of disease resistance, this hypothesis has been given little attention in wild populations. Here, we leveraged pedigree data from a barn owl (Tyto alba) population to characterize MHC haplotype structure across two MHC class I (MHC-I) and two MHC class IIB (MHC-IIB) duplicates, in order to test the hypothesis that haplotypes’ genetic diversity is higher than expected from randomly associated alleles. After showing that MHC loci are tightly linked within classes, we found limited evidence for shifts towards MHC haplotypes combining high diversity. Neither amino acid nor functional within-haplotype diversity were significantly higher than in random sets of haplotypes, regardless of MHC class. Our results therefore provide no evidence for selection towards high-diversity MHC haplotypes in barn owls. Rather, high rates of convergent evolution may constrain the evolution of high-diversity haplotypes at MHC-I, while, in contrast, for MHC-IIB, fixed differences among loci may provide barn owls with already optimized functional diversity. This suggests that at the MHC-I and MHC-IIB, respectively, different evolutionary dynamics may govern the evolution of within-haplotype diversity.

脊椎动物基因组中极高的基因复制速率与最高水平的功能等位基因多样性，是主要组织相容性复合体（major histocompatibility complex, MHC）的核心特征。作为一类在病原体识别中发挥原始作用的多基因家族，MHC的基因复制拷贝间通常存在紧密的连锁关系，这或许为单倍型的演化提供了契机——这类单倍型可将功能分化的等位基因结合在一起，进而将最优水平的多样性传递给后代。尽管这类等位基因关联或许是疾病抗性的关键组成部分，但这一假说在野生种群中尚未得到充分关注。本研究利用仓鸮（Tyto alba）种群的谱系数据，对两类MHC I类（MHC-I）与两类MHC IIB类（MHC-IIB）复制基因的单倍型结构进行表征，以验证“MHC单倍型的遗传多样性高于随机关联等位基因预期水平”这一假说。在证实MHC基因座在类内紧密连锁后，我们并未发现单倍型向高多样性组合方向偏移的明确证据。无论所属MHC类别如何，单倍型内的氨基酸多样性与功能多样性均未显著高于随机选取的单倍型组合。因此，本研究结果未为仓鸮中存在针对高多样性MHC单倍型的选择提供支持。反而，MHC I类区域较高的趋同演化速率或许限制了高多样性单倍型的演化；而与之形成对比的是，MHC IIB类的基因座间存在固定差异，这或许已为仓鸮提供了最优的功能多样性。这表明，MHC I类与MHC IIB类的单倍型内多样性演化，或许分别受到不同的演化动力学调控。