新腹足目贝类DNA条形码系统构建及系统发育研究
摘要
新腹足目隶属于腹足纲，种类繁多，其中包含约16000种海洋肉食性种类，为深海环境中一群主导性无脊椎动物类群，对海洋生态环境起着重要的调节作用。经过长期的形态演变之后，捕食行为成为新腹足目最显著的生物特征。新腹足目贝类包含大量重要的经济种类，如骨螺科、织纹螺科、塔螺科和滨螺科等经济贝类。这些经济种类都具有极其丰富的生物多样性。贝壳外部特征和消化系统解剖结构为新腹足目贝类重要的分类特征。然而，由于外部环境的影响，这些分类特征具有极大的形态可塑性，且某些群体种内差异性较大而种间差异性较小。这都使得利用传统形态特征对新腹足目贝类进行物种鉴定和系统发育分析变得极其困难，从而导致新腹足目贝类的分类处于混乱状态。
利用DNA序列进行物种多样性分析成为一种有效的研究途径。最新提出的DNA条形码（DNAbarcoding）技术，即利用一段短的DNA序列作为物种快速鉴定的标记，并希望以此建立DNA序列和生物物种之间一一对应的关系，已成功应用于动物、植物及微生物界。DNA条形码作为对地球上现有物种进行识别和鉴定的一项新技术，受到国内外广泛关注。本研究利用DNA条形码技术和相关分子标记对新腹足目贝类，特别是一些经济种类，如骨螺科和织纹螺科贝类，进行了全面的物种鉴定和系统发育研究，并验证了DNA条形码及其分析方法的有效性。研究结果如下：
1.骨螺科DNA条形码与系统发育研究
本研究中，我们运用DNA条形码技术对中国沿海17个分类比较混乱的骨螺科种类进行了物种鉴定分析。COI、16SrDNA、ITS-1和28SrRNA四个基因位点被应用于120个个体的条形码和系统发育分析。首先，由于部分骨螺个体不能用COI和16S rDNA通用引物成功扩增，我们设计出骨螺科COI和16SrDNA特异性扩增引物。研究结果显示COI基因能够成功区分所有研究种类，可以作为骨螺科理想的条形码标记基因。16SrDNA、ITS-1和28SrRNA也能够成功区分大部分研究种类，但是不能清楚鉴定一些近缘物种。另外，基于单基因数据集和整合数据集的分析结果显示爱尔螺亚科、红螺亚科、刍秣螺亚科和骨螺亚科均形成单系群，尤其是红螺亚科独自形成一单系群。本研究利用多基因位点并结合形态学特征对骨螺科种类，特别是一些经济种类，进行了有效的物种鉴定，对骨螺科种类的生态学、群体学、养殖学等研究提供了有力的分类依据。
2.织纹螺属（Nassarius）贝类隐存多样性研究
本研究对中国沿海22个织纹螺属种类的220个个体进行了全面的DNA条形码分析。其中，我们从中国沿海采集到208个织纹螺个体，并对其进行COI和16S rDNA序列的扩增与测序，其他个体序列从Genbank下载获得。距离法、单系法和特征法条形码分析方法在本研究中得到成功的应用。但是相比距离法和单系法，特征法更具优越性。研究结果表明COI和16S rDNA邻接树及贝叶斯树都显示织纹螺属为单系群体。结合线粒体序列、核基因序列及形态特征，我们成功鉴定出13个织纹螺种类，并揭示出4个隐存种和一对同物异名种类。如此成功的物种鉴定及隐存种发现对于织纹螺属的食品安全问题和多样性保护具有重大的意义，并提醒我们要更加关注被忽略的海洋隐存多样性现象。
3.新腹足目贝类分子系统发育研究
本研究首次在国内外运用多基因位点相结合（部分CO1、16S、12S、H3部分序列和18S全序列）对大量的新腹足目样本（13个科）和外群体（15个科）进行了全面的系统发育分析。运用最大简约法、最大似然法和贝叶斯方法对所得序列进行了进化树的构建。研究结果表明新腹足目为一个单系群体，其同形态学研究结果相一致，验证了运用相关形态学特征对新腹足目进行系统发育分析的有效性，并推翻了过去分子研究中新腹足目为并系或多系群体的观点。过去的分子研究由于运用有限的基因位点和分析样本而缺乏说服力。本研究结果还显示鹑螺总科和琵琶螺总科形成一个单系，并作为新腹足目的姐妹群。这一结果支持了新腹足目起源于高层中腹足目的假设。新腹足目内各个科之间的关系也在本研究中得到了厘清。除了滨螺科、塔螺科和细带螺科为并系或多系群体外，其他所有科均显示为单系群。本研究首次对新腹足目这一大海洋生物类群的进化地位进行了系统而全新的定位。
4. DNA条形码分析方法的比较研究
为了检测三种DNA条形码分析方法的有效性，即单系法、距离法和特征法（Distance,monophyly, and character–based barcoding methods），我们分别从科、属、种分类水平对40个新腹足目贝类物种的COI和16S rDNA序列进行了条形码分析。研究结果显示：（1）距离分析法不能有效的区分大部分种类，特别对于一些近缘种类，种内和种间遗传距离出现明显的重叠区，没有理想的条形码间隙（barcodinggap）出现；（2）COI邻接树比16SrDNA邻接树可以更有效的区分所研究种类，但不能有效区分一些近缘种类；（3）对于COI和16S rDNA基因，特征分析法均可以正确鉴定所有研究的新腹足目种类，并且可以有效区分一些属。此研究证明DNA条形码特征分析方法可以对不同水平的物种分类单元进行有效的区分和鉴定，特别是对于近缘物种。其次，相比距离法和单系法，特征法DNA条形码可以运用相对保守的基因片段进行条形码分析，更具优越性。
The order Neogastropoda (Gastropoda: Caenogastropoda) represents a species rich (approx.16,000living species) marine invertebrate gastropod group and has adapted to almost every marineenvironment. It contains many well-known, diverse, and ecologically significant families (such asMuricidae, Nassariidae, Turridae and Littorinidae) and has a well-established morphologicaltaxonomic system. However, the identification of neogastropod taxa is often difficult since themorphological characters (shell characters and the anatomy of the digestive system) that speciesidentification bases on are not only varied within groups but also easily to be impacted byenvironment.
DNA barcoding has been proposed as a method that will make species identification faster andmore accessible using a small fragment of DNA sequence, particularly in species with complexaccessible morphology, and has been successfully used in animals, plants and microorganism. Thisstudy employs DNA barcoding and some molecular markers to study the species identification andphylogeny of Neogastropoda, especially for the economic species of Muricidae and Nassarius.
1. DNA barcoding and phylogeny of Muricidae
This study employs a DNA barcoding method to identify17known and easily confused muricidspecies (120individuals) from the whole China coast based on mitochondrial cytochrome c oxidasesubunit I (COI) and16S rDNA sequences, and nuclear ITS-1and28S rRNA sequences. Thephylogeny of muricid subfamilies is also analysed based on all mitochondrial and nuclear sequences.The universal COI and16S rDNA primers did not work broadly across the study group, necessitatingthe redesign of muricid specific COI and16S rDNA primers. This study demonstrates that COI geneis a suitable marker for barcoding muricids, which can distinguish all muricid species studied.Phylogenetic analysis of16S rDNA, ITS-1and28S rRNA data also provide good support for thespecies resolution observed in COI data. The relationships of muricid subfamilies are resolved based on the separate and combined gene data that showed the monophyly of each the subfamiliesErgalataxinae, Rapaninae, Ocenebrinae and Muricinae, especially that Ergalataxinae did not fallwithin Rapaninae.
2. Cryptic diversity in Nassarius
This study reported a comprehensive barcoding analysis of22Nassarius species. Themitochondrial and nuclear sequences and the morphological characters are integrated to determine13Nassarius species studied and reveal four cryptic species and one pair synonyms. Distance,monophyly, and character–based barcoding methods were employed. Such successful identificationand unexpected cryptic discovery is significant for Nassarius in food safety and species conversationand remind us to pay more attention to the hidden cryptic biodiversity ignored in marine life. Distance,monophyly, and character–based barcoding methods are all very helpful in identification but thecharacter-based method shows some advantages.
3. Molecular phylogeny of Neogastropoda
This study reports the most extensive molecular study of the group published to date with increasedneogastropod taxa, multiple representatives of caenogastropod outgroups, and additional genesequences. Data were collected from the entire18S rRNA, histone H3, and three partialmitochondrial genes. Maximum parsimony, maximum likelihood and Bayesian analyses wereconducted. In the caenogastropod phylogenetic framework, Hypsogastropoda was contradictedowing to the inclusion of Cerithioidea. Contrary to previous molecular studies, all the resultsrecovered Neogastropoda as a monophyletic group, which confirms the monophyly ofNeogastropoda and the validity of morphological synapomorphies that usually define Neogastropodaas monophyletic. Tonnoidea was shown to be paraphyletic with respect to Ficidae, and together thisgroup formed a monophyletic clade as the sister group to Neogastropoda, which supported the ‘‘highmesogastropod’’ hypothesis of the origin of Neogastropoda. All neogastropod families were strongly supported except Buccinidae, Turridae and Cancellariidae. This study shed light on the status ofNeogastropoda, a controversial group, within Caenogastropoda.
4. Comparing the usefulness of DNA barcoding methods
This study analyzed108COI and10216S rDNA sequences of40species of Neogastropoda froma wide phylogenetic range to assess the performance of distance, monophyly and character-basedmethods of DNA barcoding. The distance-based method for both COI and16S rDNA genesperformed poorly in terms of species identification. Obvious overlap between intraspecific andinterspecific divergences for both genes was found. The ‘‘10×rule’’ threshold resulted in lumpingabout half of distinct species for both genes. The neighbour-joining phylogenetic tree of COI coulddistinguish all species studied. However, the16S rDNA tree could not distinguish some closelyrelated species. In contrast, the character-based barcode method for both genes successfully identified100%of the neogastropod species included, and performed well in discriminating neogastropodgenera. This present study demonstrates the effectiveness of the character-based barcoding method forspecies identification in different taxonomic levels, especially for discriminating the closely relatedspecies. While distance-and monophyly-based methods commonly use COI as the ideal gene forbarcoding, the character-based approach can perform well for species identification using relativelyconserved gene markers (e.g.,16S rDNA in this study). Nevertheless, distance and monophyly-basedmethods, especially the monophyly-based method, can still be used to flag species.
利用DNA序列进行物种多样性分析成为一种有效的研究途径。最新提出的DNA条形码（DNAbarcoding）技术，即利用一段短的DNA序列作为物种快速鉴定的标记，并希望以此建立DNA序列和生物物种之间一一对应的关系，已成功应用于动物、植物及微生物界。DNA条形码作为对地球上现有物种进行识别和鉴定的一项新技术，受到国内外广泛关注。本研究利用DNA条形码技术和相关分子标记对新腹足目贝类，特别是一些经济种类，如骨螺科和织纹螺科贝类，进行了全面的物种鉴定和系统发育研究，并验证了DNA条形码及其分析方法的有效性。研究结果如下：
1.骨螺科DNA条形码与系统发育研究
本研究中，我们运用DNA条形码技术对中国沿海17个分类比较混乱的骨螺科种类进行了物种鉴定分析。COI、16SrDNA、ITS-1和28SrRNA四个基因位点被应用于120个个体的条形码和系统发育分析。首先，由于部分骨螺个体不能用COI和16S rDNA通用引物成功扩增，我们设计出骨螺科COI和16SrDNA特异性扩增引物。研究结果显示COI基因能够成功区分所有研究种类，可以作为骨螺科理想的条形码标记基因。16SrDNA、ITS-1和28SrRNA也能够成功区分大部分研究种类，但是不能清楚鉴定一些近缘物种。另外，基于单基因数据集和整合数据集的分析结果显示爱尔螺亚科、红螺亚科、刍秣螺亚科和骨螺亚科均形成单系群，尤其是红螺亚科独自形成一单系群。本研究利用多基因位点并结合形态学特征对骨螺科种类，特别是一些经济种类，进行了有效的物种鉴定，对骨螺科种类的生态学、群体学、养殖学等研究提供了有力的分类依据。
2.织纹螺属（Nassarius）贝类隐存多样性研究
本研究对中国沿海22个织纹螺属种类的220个个体进行了全面的DNA条形码分析。其中，我们从中国沿海采集到208个织纹螺个体，并对其进行COI和16S rDNA序列的扩增与测序，其他个体序列从Genbank下载获得。距离法、单系法和特征法条形码分析方法在本研究中得到成功的应用。但是相比距离法和单系法，特征法更具优越性。研究结果表明COI和16S rDNA邻接树及贝叶斯树都显示织纹螺属为单系群体。结合线粒体序列、核基因序列及形态特征，我们成功鉴定出13个织纹螺种类，并揭示出4个隐存种和一对同物异名种类。如此成功的物种鉴定及隐存种发现对于织纹螺属的食品安全问题和多样性保护具有重大的意义，并提醒我们要更加关注被忽略的海洋隐存多样性现象。
3.新腹足目贝类分子系统发育研究
本研究首次在国内外运用多基因位点相结合（部分CO1、16S、12S、H3部分序列和18S全序列）对大量的新腹足目样本（13个科）和外群体（15个科）进行了全面的系统发育分析。运用最大简约法、最大似然法和贝叶斯方法对所得序列进行了进化树的构建。研究结果表明新腹足目为一个单系群体，其同形态学研究结果相一致，验证了运用相关形态学特征对新腹足目进行系统发育分析的有效性，并推翻了过去分子研究中新腹足目为并系或多系群体的观点。过去的分子研究由于运用有限的基因位点和分析样本而缺乏说服力。本研究结果还显示鹑螺总科和琵琶螺总科形成一个单系，并作为新腹足目的姐妹群。这一结果支持了新腹足目起源于高层中腹足目的假设。新腹足目内各个科之间的关系也在本研究中得到了厘清。除了滨螺科、塔螺科和细带螺科为并系或多系群体外，其他所有科均显示为单系群。本研究首次对新腹足目这一大海洋生物类群的进化地位进行了系统而全新的定位。
4. DNA条形码分析方法的比较研究
为了检测三种DNA条形码分析方法的有效性，即单系法、距离法和特征法（Distance,monophyly, and character–based barcoding methods），我们分别从科、属、种分类水平对40个新腹足目贝类物种的COI和16S rDNA序列进行了条形码分析。研究结果显示：（1）距离分析法不能有效的区分大部分种类，特别对于一些近缘种类，种内和种间遗传距离出现明显的重叠区，没有理想的条形码间隙（barcodinggap）出现；（2）COI邻接树比16SrDNA邻接树可以更有效的区分所研究种类，但不能有效区分一些近缘种类；（3）对于COI和16S rDNA基因，特征分析法均可以正确鉴定所有研究的新腹足目种类，并且可以有效区分一些属。此研究证明DNA条形码特征分析方法可以对不同水平的物种分类单元进行有效的区分和鉴定，特别是对于近缘物种。其次，相比距离法和单系法，特征法DNA条形码可以运用相对保守的基因片段进行条形码分析，更具优越性。
The order Neogastropoda (Gastropoda: Caenogastropoda) represents a species rich (approx.16,000living species) marine invertebrate gastropod group and has adapted to almost every marineenvironment. It contains many well-known, diverse, and ecologically significant families (such asMuricidae, Nassariidae, Turridae and Littorinidae) and has a well-established morphologicaltaxonomic system. However, the identification of neogastropod taxa is often difficult since themorphological characters (shell characters and the anatomy of the digestive system) that speciesidentification bases on are not only varied within groups but also easily to be impacted byenvironment.
DNA barcoding has been proposed as a method that will make species identification faster andmore accessible using a small fragment of DNA sequence, particularly in species with complexaccessible morphology, and has been successfully used in animals, plants and microorganism. Thisstudy employs DNA barcoding and some molecular markers to study the species identification andphylogeny of Neogastropoda, especially for the economic species of Muricidae and Nassarius.
1. DNA barcoding and phylogeny of Muricidae
This study employs a DNA barcoding method to identify17known and easily confused muricidspecies (120individuals) from the whole China coast based on mitochondrial cytochrome c oxidasesubunit I (COI) and16S rDNA sequences, and nuclear ITS-1and28S rRNA sequences. Thephylogeny of muricid subfamilies is also analysed based on all mitochondrial and nuclear sequences.The universal COI and16S rDNA primers did not work broadly across the study group, necessitatingthe redesign of muricid specific COI and16S rDNA primers. This study demonstrates that COI geneis a suitable marker for barcoding muricids, which can distinguish all muricid species studied.Phylogenetic analysis of16S rDNA, ITS-1and28S rRNA data also provide good support for thespecies resolution observed in COI data. The relationships of muricid subfamilies are resolved based on the separate and combined gene data that showed the monophyly of each the subfamiliesErgalataxinae, Rapaninae, Ocenebrinae and Muricinae, especially that Ergalataxinae did not fallwithin Rapaninae.
2. Cryptic diversity in Nassarius
This study reported a comprehensive barcoding analysis of22Nassarius species. Themitochondrial and nuclear sequences and the morphological characters are integrated to determine13Nassarius species studied and reveal four cryptic species and one pair synonyms. Distance,monophyly, and character–based barcoding methods were employed. Such successful identificationand unexpected cryptic discovery is significant for Nassarius in food safety and species conversationand remind us to pay more attention to the hidden cryptic biodiversity ignored in marine life. Distance,monophyly, and character–based barcoding methods are all very helpful in identification but thecharacter-based method shows some advantages.
3. Molecular phylogeny of Neogastropoda
This study reports the most extensive molecular study of the group published to date with increasedneogastropod taxa, multiple representatives of caenogastropod outgroups, and additional genesequences. Data were collected from the entire18S rRNA, histone H3, and three partialmitochondrial genes. Maximum parsimony, maximum likelihood and Bayesian analyses wereconducted. In the caenogastropod phylogenetic framework, Hypsogastropoda was contradictedowing to the inclusion of Cerithioidea. Contrary to previous molecular studies, all the resultsrecovered Neogastropoda as a monophyletic group, which confirms the monophyly ofNeogastropoda and the validity of morphological synapomorphies that usually define Neogastropodaas monophyletic. Tonnoidea was shown to be paraphyletic with respect to Ficidae, and together thisgroup formed a monophyletic clade as the sister group to Neogastropoda, which supported the ‘‘highmesogastropod’’ hypothesis of the origin of Neogastropoda. All neogastropod families were strongly supported except Buccinidae, Turridae and Cancellariidae. This study shed light on the status ofNeogastropoda, a controversial group, within Caenogastropoda.
4. Comparing the usefulness of DNA barcoding methods
This study analyzed108COI and10216S rDNA sequences of40species of Neogastropoda froma wide phylogenetic range to assess the performance of distance, monophyly and character-basedmethods of DNA barcoding. The distance-based method for both COI and16S rDNA genesperformed poorly in terms of species identification. Obvious overlap between intraspecific andinterspecific divergences for both genes was found. The ‘‘10×rule’’ threshold resulted in lumpingabout half of distinct species for both genes. The neighbour-joining phylogenetic tree of COI coulddistinguish all species studied. However, the16S rDNA tree could not distinguish some closelyrelated species. In contrast, the character-based barcode method for both genes successfully identified100%of the neogastropod species included, and performed well in discriminating neogastropodgenera. This present study demonstrates the effectiveness of the character-based barcoding method forspecies identification in different taxonomic levels, especially for discriminating the closely relatedspecies. While distance-and monophyly-based methods commonly use COI as the ideal gene forbarcoding, the character-based approach can perform well for species identification using relativelyconserved gene markers (e.g.,16S rDNA in this study). Nevertheless, distance and monophyly-basedmethods, especially the monophyly-based method, can still be used to flag species.
引文
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