Selfish genetic elements comprise significant fractions of mammalian genomes. In rare instances, host genomes domesticate segments of these elements for function. Using a complete human genome assembly and 25 additional vertebrate genomes, we re-analyzed the evolutionary trajectories and functional potential of capsid genes domesticated from Metaviridae, a lineage of retrovirus-like retrotransposons. Our study expands on previous analyses to unearth several new insights about the evolutionary histories of these ancient genes. We find that at least five independent domestication events occurred from diverse Metaviridae, giving rise to three universally-retained single-copy genes evolving under purifying selection and two gene families unique to placental mammals with multiple members showing evidence of rapid evolution. In the SIRH/RTL family, we find diverse amino-terminal domains, widespread loss of protein-coding capacity in RTL10 despite its retention in several mammalian lineages, and differential utilization of an ancient programmed ribosomal frameshift in RTL3 between the domesticated capsid and protease domains. Our analyses also reveal that most members of the PNMA family in mammalian genomes encode a conserved putative amino-terminal RNA-binding domain both adjoining and independent from domesticated capsid domains. Our analyses lead to a significant correction of previous annotations of the essential CCDC8 gene. We show that this putative RNA-binding domain is also present in several extant Metaviridae, revealing a novel protein domain configuration in retrotransposons. Collectively, our study reveals the divergent outcomes of multiple domestication events from diverse Metaviridae in the common ancestor of placental mammals.

中文翻译：

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哺乳动物驯化后病毒衣壳基因的不同进化史

自私的遗传元素构成了哺乳动物基因组的重要部分。在极少数情况下，宿主基因组会驯化这些元件的片段以发挥功能。利用完整的人类基因组组装和另外 25 个脊椎动物基因组，我们重新分析了从 Metaviridae（一种逆转录病毒样逆转录转座子谱系）驯化的衣壳基因的进化轨迹和功能潜力。我们的研究扩展了之前的分析，以发掘有关这些古老基因进化历史的一些新见解。我们发现，不同的后病毒科动物至少发生了五个独立的驯化事件，产生了在纯化选择下进化的三个普遍保留的单拷贝基因，以及胎盘哺乳动物特有的两个基因家族，其中多个成员显示出快速进化的证据。在 SIRH/RTL 家族中，我们发现了不同的氨基末端结构域，RTL10 中蛋白质编码能力的广泛丧失，尽管它保留在几个哺乳动物谱系中，以及驯化衣壳和蛋白酶结构域之间对 RTL3 中古老程序化核糖体移码的差异利用。我们的分析还表明，哺乳动物基因组中 PNMA 家族的大多数成员编码保守的推定氨基末端 RNA 结合结构域，该结构域与驯化衣壳结构域相邻且独立。我们的分析对关键 CCDC8 基因之前的注释进行了重大修正。我们发现这种假定的 RNA 结合结构域也存在于几种现存的后病毒科中，揭示了反转录转座子中的一种新的蛋白质结构域配置。总的来说，我们的研究揭示了胎盘哺乳动物共同祖先中不同后病毒科的多次驯化事件的不同结果。