The evolution of microRNAs (miRNAs) has been studied extensively to understand their roles in gene regulation and evolutionary processes. This review focuses on how miRNA-mediated regulation has evolved in bilaterian animals, highlighting both convergent and divergent evolution. Since animals and plants display significant differences in miRNA biogenesis and target recognition, the ‘independent origin’ hypothesis proposes that miRNA pathways in these groups independently evolved from the RNA interference (RNAi) pathway, leading to modern miRNA repertoires through convergent evolution. However, recent evidence raises the alternative possibility that the miRNA pathway might have already existed in the last common ancestor of eukaryotes, and that the differences in miRNA pathway and miRNA repertoires among animal and plant lineages arise from lineage-specific innovations and losses of miRNA pathways, miRNA acquisition, and loss of miRNAs after eukaryotic divergence. The repertoire of miRNAs has considerably expanded during bilaterian evolution, primarily through de novo creation and duplication processes, generating new miRNAs. Although ancient functionally established miRNAs are rarely lost, many newly emerged miRNAs are transient and lineage specific, following a birth–death evolutionary pattern aligning with the ‘out-of-the-testis’ and ‘transcriptional control’ hypotheses. Our focus then shifts to the convergent molecular evolution of miRNAs. We summarize how miRNA clustering and seed mimicry contribute to this phenomenon, and we review how miRNAs from different sources converge to degrade maternal messenger RNAs (mRNAs) during animal development. Additionally, we describe how miRNAs evolve across species due to changes in sequence, seed shifting, arm switching, and spatiotemporal expression patterns, which can result in variations in target sites among orthologous miRNAs across distant strains or species. We also provide a summary of the current understanding regarding how the target sites of orthologous miRNAs can vary across strains or distantly related species. Although many paralogous miRNAs retain their seed or mature sequences after duplication, alterations can occur in the seed or mature sequences or expression patterns of paralogous miRNAs, leading to functional diversification. We discuss our current understanding of the functional divergence between duplicated miRNAs, and illustrate how the functional diversification of duplicated miRNAs impacts target site evolution. By investigating these topics, we aim to enhance our current understanding of the functions and evolutionary dynamics of miRNAs. Additionally, we shed light on the existing challenges in miRNA evolutionary studies, particularly the complexity of deciphering the role of miRNA-mediated regulatory network evolution in shaping gene expression divergence and phenotypic differences among species.

中文翻译：

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后生动物中 microRNA 介导的趋同和趋异进化

人们对 microRNA (miRNA) 的进化进行了广泛的研究，以了解它们在基因调控和进化过程中的作用。本综述重点关注两侧对称动物中 miRNA 介导的调控如何进化，强调趋同进化和趋异进化。由于动物和植物在 miRNA 生物发生和靶标识别方面表现出显着差异，“独立起源”假说提出，这些群体中的 miRNA 通路是从 RNA 干扰 (RNAi) 通路独立进化而来，通过趋同进化形成现代 miRNA 库。然而，最近的证据提出了另一种可能性，即 miRNA 通路可能已经存在于真核生物的最后一个共同祖先中，并且动物和植物谱系之间 miRNA 通路和 miRNA 库的差异源于谱系特异性的创新和 miRNA 通路的丢失、 miRNA 的获得以及真核生物分化后 miRNA 的丢失。在两侧对称动物进化过程中，miRNA 的种类显着扩展，主要是通过从头创建和复制过程，产生新的 miRNA。尽管古老的功能确立的 miRNA 很少丢失，但许多新出现的 miRNA 是短暂的和谱系特异性的，遵循与“睾丸外”和“转录控制”假设一致的出生-死亡进化模式。然后我们的重点转向 miRNA 的趋同分子进化。我们总结了 miRNA 聚类和种子拟态如何导致这种现象，并回顾了不同来源的 miRNA 在动物发育过程中如何聚合降解母体信使 RNA (mRNA)。此外，我们描述了 miRNA 如何因序列、种子移位、臂转换和时空表达模式的变化而在物种之间进化，这可能导致远缘菌株或物种的直系同源 miRNA 之间的靶位点发生变化。我们还总结了目前关于直向同源 miRNA 的靶位点如何在菌株或远缘相关物种之间变化的理解。尽管许多旁系同源 miRNA 在复制后保留其种子或成熟序列，但旁系同源 miRNA 的种子或成熟序列或表达模式可能发生改变，从而导致功能多样化。我们讨论了目前对重复 miRNA 之间功能差异的理解，并说明了重复 miRNA 的功能多样性如何影响靶位点进化。通过研究这些主题，我们的目标是增强我们目前对 miRNA 的功能和进化动力学的理解。此外，我们还阐明了 miRNA 进化研究中现有的挑战，特别是破译 miRNA 介导的调控网络进化在塑造基因表达差异和物种间表型差异方面的作用的复杂性。