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，高基因重复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；该多基因家族在病原体识别中发挥基础性作用。MHC基因重复序列间普遍存在的紧密连锁，可能为单倍型的演化提供契机——这类单倍型可结合功能分化的等位基因，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2个MHC I类（MHC-I）与2个MHC IIB类（MHC-IIB）基因重复序列的单倍型结构进行解析，以检验“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基因座在各自类别内紧密连锁后，我们仅发现有限证据支持选择偏向于兼具高多样性的MHC单倍型这一趋势。无论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集合。因此，本研究结果未发现仓鸮存在针对高多样性MHC单倍型的选择信号。相反，MHC-I区域较高的趋同演化速率或许会限制高多样性单倍型的演化；而与之形成对比的是，MHC-IIB区域基因座间的固定差异，或许已为仓鸮提供了优化的功能多样性。这表明，MHC-I与MHC-IIB区域的单倍型内多样性演化，或许分别受不同的演化动力所调控。