Taxonomy, phylogeny and evolution of freshwater mussels (Unionoida: Unionoidea) in China revealed by multilocus phylogenetic analyses and mitochondrial phylogenomics

Abstract

中国是东亚蚌类（蚌目：蚌超科）物种分布中心，共记录有26属.然而，在世界蚌目框架下，中国仍缺乏一个完整科学的蚌类分类系统.本研究基于多位点分子标记（COI、16S、28S）和线粒体基因组学重构聚焦于蚌超科的蚌目系统发育关系，ML、BI和BEAST系统发育结果均支持蚌科5亚科分类系统，即（（（Ambleminae+Gonideinae）+Rectidentinae）+Unioninae）+Parreysiinae；珍珠蚌科2亚科分类系统，即（Gibbosulinae+Margaritiferinae）；中国蚌类隶属蚌科4亚科（Gonideinae，Rectidentinae，Unioninae，Parreysiinae）13族和珍珠蚌科两亚科（Gibbosulinae，Margaritiferinae）.基于化石标定的分子钟显示：蚌科物种分化时间为中三叠世（median=232.07 Ma），其中雕刻蚌亚科（Parreysiinae）起源和物种分化时间早于其他亚科；矩形蚌亚科（Rectidentinae）物种分化时间最晚，为晚白垩世（median=94.72 Ma）；小方蚌亚科（Ambleminae）和隆脊蚌亚科（Gonideinae）最近共同祖先分化于晚侏罗纪世（median=144.69 Ma），珍珠蚌科起源于晚石炭世（median=312.61 Ma），物种分化于晚白垩世（median=91.59 Ma），中国蚌科现生物种最早起源时间可追溯到白垩纪（中国尖嵴蚌（Acuticosta chinensis），median=114.36 Ma）.蚌超科线粒体基因重排分析显示：蚌超科线粒体基因组有4种基因排列方式（GO），珍珠蚌科独享一种（GO1）；蚌科中Unioninae和Ambleminae共享一种（GO2）；Gonideinae有2种基因排列方式（GO3和GO4），其中室蚌（Chamberlainia hainesiana）独享一种（GO4），其余物种共享一种（GO3）.以往作为高阶元分类的贝壳形态、钩介幼虫形态以及育儿囊类型，并不能作为蚌科属及以上阶元分类依据.本研究重构了世界蚌目聚焦于蚌超科的系统发育关系和进化历史，建立了中国蚌类分类系统，为今后该类群区系多样性研究及资源保护提供了分类依据.;China is the most species-rich region for the Unionoidea (Unionidae + Margaritiferidae) in East Asia, with a total of 26 genera. However, in the context of global unionids, an integrated and scientific phylogenetic taxonomy for Chinese Unionoidea is still lack. Based on the multilocus molecular markers (COI, 16S, 28S) and mitochondrial genomics, we reconstructed the phylogenetic relationship of the Unionioda by focusing on the Unionoidea. All phylogenetic results of ML, BI and BEAST supported five monophyletic clades for subfamily levels within Unionidae, i.e. (((Ambleminae + Gonideinae) + Rectidentinae) + Unioninae) + Parreysiinae, and two subfamilies within Margaritiferidae, i.e. (Gibbosulinae + Margaritiferinae). Chinese Unionoidea belonged to four subfamilies (Gonideinae, Rectidentinae, Unioninae, Parreysiinae) thirteen tribes of Unionidae and 2 subfamilies (Gibbosulinae, Margaritiferinae) of Margaritiferidae. The fossil-calibrated molecular clock suggested the Unionidae species divergence at the Middle Triassic (median=232.07 Ma). The origin and species divergence time of the Parreysiinae were earlier than other subfamilies. The species divergence time of Rectidentinae was the latest among all subfamilies, at the Late Cretaceous (median=94.72 Ma). The most recently common ancestor of Ambleminae and Gonideinae diverged at the Late Jurassic (median=144.69 Ma). Margaritiferidae originated at the Late Carboniferous (median=312.61 Ma), and species divergence at the Late Cretaceous (median=91.59 Ma). The oldest living unionid species in China could be traced back to the Cretaceous (i.e. Acuticosta chinensis, median=114.36 Ma). Mitochondrial gene order (GO) analysis of the Unionoidea revealed that the presently published Unionoidea mitochondrial genome had four gene arrangements:one was exclusive to the Margaritiferidae (GO1); Unioninae and Ambleminae of Unionidae shared another one (GO2); Gonideinae had two gene arrangements (GO3 and GO4), of which was exclusive to Chamberlainia hainesiana (GO4). The morphological features of shells, glochidia and marsupium, which were used to high-level classification, could not be regarded as diagnostic features for the subfamily and the tribe level. This study reconstructed the phylogenetic relationship and evolutionary history of Unionoida worldwide and established complete systematics of Unionoidea in China, which providing the taxonomic basis for the diversity research and resource conservation of Chinese unionids.