Strong mitonuclear discordance in the phylogeny of Neodermata and evolutionary rates of Polyopisthocotylea

IF 3.7 2区 医学 Q1 PARASITOLOGY International journal for parasitology Pub Date : 2024-04-01 DOI:10.1016/j.ijpara.2024.01.001
Dong Zhang , Ivan Jakovlić , Hong Zou , Fei Liu , Chuan-Yu Xiang , Qunzong Gusang , Sonam Tso , Shenggui Xue , Wen-Jin Zhu , Zhenxin Li , Jihua Wu , Gui-Tang Wang
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Abstract

The genomic evolution of Polyopisthocotylea remains poorly understood in comparison to the remaining three classes of Neodermata: Monopisthocotylea, Cestoda, and Trematoda. Moreover, the evolutionary sequence of major events in the phylogeny of Neodermata remains unresolved. Herein we sequenced the mitogenome and transcriptome of the polyopisthocotylean Diplorchis sp., and conducted comparative evolutionary analyses using nuclear (nDNA) and mitochondrial (mtDNA) genomic datasets of Neodermata. We found strong mitonuclear discordance in the phylogeny of Neodermata. Polyopisthocotylea exhibited striking mitonuclear discordance in relative evolutionary rates: the fastest-evolving mtDNA in Neodermata and a comparatively slowly-evolving nDNA genome. This was largely attributable to its very long stem branch in mtDNA topologies, not exhibited by the nDNA data. We found indications that the fast evolution of mitochondrial genomes of Polyopisthocotylea may be driven both by relaxed purifying selection pressures and elevated levels of directional selection. We identified mitochondria-associated genes encoded in the nuclear genome: they exhibited unique evolutionary rates, but not correlated with the evolutionary rate of mtDNA, and there is no evidence for compensatory evolution (they evolved slower than the rest of the genome). Finally, there appears to exist an exceptionally large (≈6.3 kb) nuclear mitochondrial DNA segment (numt) in the nuclear genome of newly sequenced Diplorchis sp. A 3′-end segment of the 16S rRNA gene encoded by the numt was expressed, suggesting that this gene acquired novel, regulatory functions after the transposition to the nuclear genome. In conclusion, Polyopisthocotylea appears to be the lineage with the fastest-evolving mtDNA sequences among all of Bilateria, but most of the substitutions were accumulated deep in the evolutionary history of this lineage. As the nuclear genome does not exhibit a similar pattern, the circumstances underpinning this evolutionary phenomenon remain a mystery.

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新皮层动物系统发育中的强有丝分裂核不一致性与多皮层动物的进化速度
与其余三类新真皮动物(单真皮动物、绦虫纲和吸虫纲)相比,人们对多毛目动物的基因组进化仍然知之甚少。此外,新真皮纲系统发育过程中主要事件的进化顺序仍未确定。在本文中,我们测序了多肉纲 Diplorchis sp.的有丝分裂基因组和转录组,并利用新皮目动物的核(nDNA)和线粒体(mtDNA)基因组数据集进行了比较进化分析。我们发现,新皮目动物的系统进化中存在强烈的有丝分裂核不一致性。多肉植物在相对进化速度上表现出惊人的有丝分裂核不一致性:在新皮类中,mtDNA的进化速度最快,而nDNA基因组的进化速度相对较慢。这在很大程度上归因于其 mtDNA 拓扑中很长的茎枝,而 nDNA 数据则没有表现出这一点。我们发现有迹象表明,多肉植物线粒体基因组的快速进化可能是由宽松的纯化选择压力和高水平的定向选择共同驱动的。我们发现了核基因组中编码的线粒体相关基因:它们表现出独特的进化速度,但与 mtDNA 的进化速度不相关,也没有补偿性进化的证据(它们的进化速度慢于基因组的其他部分)。最后,在新测序的Diplorchis sp.的核基因组中似乎存在一个特别大(≈6.3 kb)的线粒体DNA核片段(numt),由numt编码的16S rRNA基因的3'端片段被表达,表明该基因在转位到核基因组后获得了新的调控功能。总之,在所有双子叶植物中,多肉植物似乎是mtDNA序列进化最快的一个品系,但大部分的替换是在该品系进化史的深处积累起来的。由于核基因组没有表现出类似的模式,这种进化现象的基础情况仍然是一个谜。
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来源期刊
CiteScore
8.40
自引率
2.50%
发文量
76
审稿时长
23 days
期刊介绍: International Journal for Parasitology offers authors the option to sponsor nonsubscriber access to their articles on Elsevier electronic publishing platforms. For more information please view our Sponsored Articles page. The International Journal for Parasitology publishes the results of original research in all aspects of basic and applied parasitology, including all the fields covered by its Specialist Editors, and ranging from parasites and host-parasite relationships of intrinsic biological interest to those of social and economic importance in human and veterinary medicine and agriculture.
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