Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes

Animals have fascinating diversity of life forms. Analyses of the available genome sequence reveals dynamic evolution of gene gain and loss at different lineages in the animal tree of life (e.g. Albalat and Canestro 2016; Sharma et al 2018; Fernandez and Gabaldon 2020; Guijarro-Clarke et al 2020; Jebb et al 2020). Gene gain via another kingdom as well as the evolutionary consequence of gene loss are generally ignored and difficult to interpret. Here we sequenced six new myriapod genomes at key phylogenetic positions of this understudied arthropod lineage (three millipedes and three centipedes). Comparison of myriapod genomes revealed multiple horizontal gene transfer (HGT) of genes shared between centipedes, including <i>glucose/arabinose dehydrogenase</i> that happened at the last common of ancestor of centipedes, while there was no detectable HGT shared between the millipedes. In all millipede lineages, the loss of <i>juvenile hormone O-methyltransferase</i>, a key enzyme in catalysing the last step of sesquiterpenoid hormone methyl farnesoate production in arthropods was revealed. These findings provided the first evidence of shared HGT in the last common ancestor of centipede ancestor, while gene loss event could indeed happen in endocrine system in contrary to the conventional view of stepwise gene gain resulting in diversity of animal physiology for adaptation to environment.动物界拥有令人惊叹的生命形式多样性。现有基因组序列分析显示，动物生命之树的不同支系均存在动态的基因得失演化过程（如Albalat与Canestro，2016；Sharma等，2018；Fernandez与Gabaldon，2020；Guijarro-Clarke等，2020；Jebb等，2020）。通过跨界途径获得基因，以及基因丢失的演化效应，长期以来常被忽视且难以阐释。本研究针对这一研究较少的多足类节肢动物支系的关键系统发育位置，测序获得6个全新的多足类基因组（3个马陆基因组与3个蜈蚣基因组）。对多足类基因组的比较分析显示，蜈蚣类群间存在多起共享的水平基因转移（horizontal gene transfer, HGT）事件，其中包括发生在蜈蚣最近共同祖先中的*葡萄糖/阿拉伯糖脱氢酶*相关转移事件；而马陆类群中未检测到共享的HGT事件。在所有马陆支系中，均存在*保幼激素O-甲基转移酶*的丢失——该酶是节肢动物中催化倍半萜激素法尼酸甲酯合成最后一步的关键酶。本研究发现首次提供了蜈蚣最近共同祖先存在共享HGT事件的证据，同时证实基因丢失事件确实可发生在内分泌系统中，这与传统认为“动物生理多样性由逐步基因增益以适应环境”的观点相悖。