University of Hamburg, Hamburg, Germany.
Leibniz Institute for the Analysis of Biodiversity Change, Museum of Nature, Hamburg, Germany.
Insect Mol Biol. 2023 Aug;32(4):387-399. doi: 10.1111/imb.12838. Epub 2023 Apr 1.
Mitochondrial gene order has contributed to the elucidation of evolutionary relationships in several animal groups. It generally has found its application as a phylogenetic marker for deep nodes. Yet, in Orthoptera limited research has been performed on the gene order, although the group represents one of the oldest insect orders. We performed a comprehensive study on mitochondrial genome rearrangements (MTRs) within Orthoptera in the context of mitogenomic sequence-based phylogeny. We used 280 published mitogenome sequences from 256 species, including three outgroup species, to reconstruct a molecular phylogeny. Using a heuristic approach, we assigned MTR scenarios to the edges of the phylogenetic tree and reconstructed ancestral gene orders to identify possible synapomorphies in Orthoptera. We found all types of MTRs in our dataset: inversions, transpositions, inverse transpositions, and tandem-duplication/random loss events (TDRL). Most of the suggested MTRs were in single and unrelated species. Out of five MTRs which were unique in subgroups of Orthoptera, we suggest four of them to be synapomorphies; those were in the infraorder Acrididea, in the tribe Holochlorini, in the subfamily Pseudophyllinae, and in the two families Phalangopsidae and Gryllidae or their common ancestor (leading to the relationship ((Phalangopsidae + Gryllidae) + Trigonidiidae)). However, similar MTRs have been found in distant insect lineages. Our findings suggest convergent evolution of specific mitochondrial gene orders in several species, deviant from the evolution of the mitogenome DNA sequence. As most MTRs were detected at terminal nodes, a phylogenetic inference of deeper nodes based on MTRs is not supported. Hence, the marker does not seem to aid resolving the phylogeny of Orthoptera, but adds further evidence for the complex evolution of the whole group, especially at the genetic and genomic levels. The results indicate a high demand for more research on patterns and underlying mechanisms of MTR events in Orthoptera.
线粒体基因顺序在多个动物类群的进化关系阐明中发挥了作用。它通常被用作深节点的系统发育标记。然而，在直翅目动物中，对基因顺序的研究有限，尽管该目是昆虫中最古老的目之一。我们在基于线粒体基因组序列的系统发育学背景下，对直翅目动物的线粒体基因组重排（MTR）进行了全面研究。我们使用了 256 个物种的 280 个已发表的线粒体基因组序列，包括 3 个外群物种，以重建分子系统发育关系。我们使用启发式方法将 MTR 情景分配给系统发育树的边缘，并重建祖先基因顺序，以确定直翅目动物中的可能同源特征。我们在数据集内发现了所有类型的 MTR：反转、转座、反转转座和串联重复/随机丢失事件（TDRL）。大多数建议的 MTR 都发生在单个且无关的物种中。在直翅目动物的 5 个独特的 MTR 中，我们建议其中 4 个是同源特征；它们发生在亚目 Acrididea 中、在 Holochlorini 部落中、在 Pseudophyllinae 亚科中、以及在 Phalangopsidae 和 Gryllidae 两个科或它们的共同祖先（导致关系 ((Phalangopsidae + Gryllidae) + Trigonidiidae))。然而，类似的 MTR 也在遥远的昆虫谱系中被发现。我们的研究结果表明，在几个物种中，特定的线粒体基因顺序发生了趋同进化，偏离了线粒体基因组 DNA 序列的进化。由于大多数 MTR 是在末端节点检测到的，因此基于 MTR 对更深节点的系统发育推断不被支持。因此，该标记似乎无助于解决直翅目动物的系统发育，而是为整个群体的复杂进化，特别是在遗传和基因组水平上，提供了进一步的证据。结果表明，需要对直翅目动物的 MTR 事件的模式和潜在机制进行更多的研究。
