Herlyn Holger, Hembrom Anju Angelina, Tosar Juan-Pablo, Mauer Katharina M, Schmidt Hanno, Dezfuli Bahram Sayyaf, Hankeln Thomas, Bachmann Lutz, Sarkies Peter, Peterson Kevin J, Fromm Bastian
Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany.
The Arctic University Museum of Norway, UiT-The Arctic University of Norway, Tromsø, Norway.
Genome Biol Evol. 2025 Jul 3;17(7). doi: 10.1093/gbe/evaf124.
Within the last 800 million years, animals evolved a vast range of diversity of species exhibiting an enormous disparity of forms and lifestyles. The process involved an increase in complexity from life forms with few cell types to organisms with many hundreds of cell types. However, neither genome size nor number of protein-coding genes can explain these differences, and their biological basis remains elusive. Yet, recent studies suggest that the evolution of complexity is closely linked to the acquisition of a class of noncoding gene regulators called microRNAs. To test this hypothesis, we investigated the association between loss of organismal complexity and microRNAs in Syndermata, an invertebrate group including free-living wheel animals (Monogononta, Bdelloidea), epibiotic Seisonidea, and endoparasitic thorny-headed worms (Acanthocephala). Analyses of genomic, transcriptomic, and morphological data of altogether 25 syndermatan species revealed strong correlations of microRNA losses with reductions of protein-coding genes and morphological traits. The hierarchical pattern sums up to ∼85% loss of microRNAs and a ∼50% loss of conserved metazoan core genes (Benchmarking Universal Single-Copy Orthologs) on the lineage to thorny-headed worms. Extraordinarily reduced microRNA complements were confirmed by small RNA sequencing data. Endoparasitic Acanthocephala was additionally distinguished by the most morphological reductions of ancestral features, such as the digestive tract. Together, we observed that reductions of ∼400 protein-coding genes and 10 metazoan core genes tended to accompany the loss of single microRNA families. Furthermore, 4 microRNA families and 34 metazoan core genes appeared to be associated, on average, with the reduction of a single morphological trait.
在过去的8亿年里，动物进化出了种类繁多的物种，展现出形态和生活方式的巨大差异。这个过程涉及到从细胞类型较少的生命形式到拥有数百种细胞类型的生物体的复杂性增加。然而，基因组大小和蛋白质编码基因的数量都无法解释这些差异，其生物学基础仍然难以捉摸。不过，最近的研究表明，复杂性的进化与一类称为微小RNA的非编码基因调控因子的获得密切相关。为了验证这一假设，我们研究了 Syndermata 中生物体复杂性丧失与微小RNA之间的关联，Syndermata 是一个无脊椎动物类群，包括自由生活的轮虫动物（单巢纲、蛭形轮虫纲）、体表共生的塞氏轮虫纲和内寄生的棘头虫（棘头动物门）。对总共25种 Syndermata 物种的基因组、转录组和形态学数据的分析揭示了微小RNA丢失与蛋白质编码基因和形态特征减少之间的强相关性。在进化到棘头虫的谱系上，这种层级模式总结为微小RNA约85%的丢失和后生动物核心保守基因（基准通用单拷贝直系同源基因）约50%的丢失。小RNA测序数据证实了棘头虫的微小RNA互补序列异常减少。内寄生的棘头动物门还以祖先特征（如消化道）的最大形态简化为特征。我们共同观察到，约400个蛋白质编码基因和10个后生动物核心基因的减少往往伴随着单个微小RNA家族的丢失。此外，平均而言，4个微小RNA家族和34个后生动物核心基因似乎与单个形态特征的减少有关。
