Still waters run deep: Large scale genome rearrangements in the evolution of morphologically conservative Polyplacophora

<b>Background:</b> A major question in animal evolution is how genotypic and phenotypic changes are related, and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four <i>de novo</i> assemblies, covering all major chiton clades, and an updated phylogeny for the phylum.<b>Results:</b> We constructed 20 ancient molluscan linkage groups (MLGs) that are relatively conserved in bivalve karyotypes, but subject to re-ordering, rearrangement, fusion, or partial duplication among chitons, varying even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid <i>Liolophura japonica</i> has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca.<b>Conclusions:</b> The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.

**研究背景：** 动物演化领域的核心问题之一，在于阐释基因型（genotypic）与表型（phenotypic）变化之间的关联，以及古老的基因排列是否在现存演化支（clades）中得以保留。石鳖隶属于软体动物门多板纲（Polyplacophora），其躯体构型与整体形态自古生代（Palaeozoic）以来几乎未发生显著改变。本研究对5个参考级基因组开展比较分析，其中包含4个从头组装（de novo）的基因组，覆盖了所有主要的石鳖演化支，并更新了软体动物门的系统发育关系。**研究结果：** 本研究构建了20个古老的软体动物连锁群（molluscan linkage groups, MLGs），这类连锁群在双壳类核型中相对保守，但在石鳖类群中却经历了重排、重组、融合或部分复制，甚至在同属物种间也存在差异。最具祖征性状的鳞侧石鳖目（Lepidopleurida）出现了最多的新型融合事件，而石鳖科的日本滑石鳖（Liolophura japonica）发生了部分基因组复制，这将软体动物门内大规模基因复制的发生范围进一步拓展。**研究结论：** 该纲类群所具有的极端且动态的基因组重排特征，与绝大多数其他动物类群形成鲜明对比，这表明石鳖突破了作用于其他动物类群的演化约束。石鳖看似保守的表型组（phenome），实则掩盖了其基因组层面快速且广泛的变化。