The Complete Mitochondrial Genomes of Six Heterodont Bivalves (Tellinoidea and Solenoidea): Variable Gene Arrangements and Phylogenetic Implications

BackgroundTaxonomy and phylogeny of subclass Heterodonta including Tellinoidea are long-debated issues and a complete agreement has not been reached yet. Mitochondrial (mt) genomes have been proved to be a powerful tool in resolving phylogenetic relationship. However, to date, only ten complete mitochondrial genomes of Heterodonta, which is by far the most diverse major group of Bivalvia, have been determined. In this paper, we newly sequenced the complete mt genomes of six species belonging to Heterodonta in order to resolve some problematical relationships among this subclass. Principal FindingsThe complete mt genomes of six species vary in size from 16,352 bp to 18,182. Hairpin-like secondary structures are found in the largest non-coding regions of six freshly sequenced mt genomes, five of which contain tandem repeats. It is noteworthy that two species belonging to the same genus show different gene arrangements with three translocations. The phylogenetic analysis of Heterodonta indicates that Sinonovacula constricta, distant from the Solecurtidae belonging to Tellinoidea, is as a sister group with Solen grandis of family Solenidae. Besides, all five species of Tellinoidea cluster together, while Sanguinolaria diphos has closer relationship with Solecurtus divaricatus, Moerella iridescens and Semele scaba rather than with Sanguinolaria olivacea. Conclusions/SignificanceBy comparative study of gene order rearrangements and phylogenetic relationships of the five species belonging to Tellinoidea, our results support that comparisons of mt gene order rearrangements, to some extent, are a useful tool for phylogenetic studies. Based on phylogenetic analyses of multiple protein-coding genes, we prefer classifying the genus Sinonovacula within the superfamily Solenoidea and not the superfamily Tellinoidea. Besides, both gene order and sequence data agree that Sanguinolaria (Psammobiidae) is not monophyletic. Nevertheless, more studies based on more mt genomes via combination of gene order and phylogenetic analysis are needed to further understand the phylogenetic relationships in subclass Heterodonta.

【背景】包含樱蛤总科（Tellinoidea）在内的异齿亚纲（Heterodonta）的分类与系统发育研究长期以来颇具争议，至今尚未形成统一共识。线粒体（mt）基因组已被证实为解析类群系统发育关系的高效工具。然而，作为双壳纲（Bivalvia）现今多样性最高的大类群，异齿亚纲迄今仅完成了10个完整线粒体基因组的测序组装。本研究新测定了6个异齿亚纲物种的完整线粒体基因组，旨在厘清该亚纲内部分悬而未决的系统发育关系。
【主要发现】本次新测序的6个异齿亚纲物种完整线粒体基因组长度介于16352 bp至18182 bp之间。6个基因组的最大非编码区均存在发夹状二级结构，其中5个基因组包含串联重复序列。值得关注的是，同属的两个物种间存在3处基因易位，导致二者的基因排列方式出现显著差异。针对异齿亚纲的系统发育分析结果显示：缢蛏（Sinonovacula constricta）与隶属于竹蛏科（Solenidae）的大竹蛏（Solen grandis）构成姐妹群，其与樱蛤总科（Tellinoidea）的紫云蛤科（Solecurtidae）亲缘关系较远。此外，樱蛤总科的5个物种聚为一支；而紫蛤（Sanguinolaria diphos）与橄榄紫蛤（Sanguinolaria olivacea）亲缘关系较远，反而与弯形紫云蛤（Solecurtus divaricatus）、彩虹马珂蛤（Moerella iridescens）及斯氏半纹蛤（Semele scaba）的亲缘关系更为密切。
【结论与意义】通过对樱蛤总科5个物种的基因重排模式与系统发育关系开展比较分析，本研究结果证实，线粒体基因重排比较在一定程度上可作为系统发育研究的有效辅助手段。基于多个蛋白编码基因的系统发育分析表明，应将Sinonovacula属归入竹蛏总科（Solenoidea），而非樱蛤总科。此外，基因重排与序列数据均支持紫蛤所在的紫云蛤科（Psammobiidae）并非单系群。尽管本研究取得了阶段性进展，但仍需基于更多线粒体基因组，结合基因重排与系统发育分析开展深入研究，方能进一步阐明异齿亚纲内完整的系统发育关系。