木瓜榕榕小蜂群落中Wolbachia的感染格局
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摘要
榕树（桑科：榕属）和榕小蜂（昆虫纲：膜翅目：小蜂总科）体系成为验证互利共生系统的起源与进化、资源竞争、共生体系稳定机制、性比分配等理论的经典模式之一。庞大而复杂的榕小蜂群落，以及榕小蜂极端的雌雄异型和雄性多型现象，使得榕小蜂分类工作出现种间定名混乱、雌雄不配对等问题。对此，在传统昆虫形态分类研究基础上，我们引入了DNA条形码技术，采用国际通用标准线粒体基因的cox1片段，对榕小蜂个体进行无损伤DNA提取，依据种间差异大于种内差异的原理，快速准确的鉴定榕小蜂种类。Wolbachia是广泛分布在节肢动物和一些线虫体内的内共生菌，在种系间其传播途径是从母代传给子代，可以操纵寄主生殖，如胞质不相容、孤雌生殖、雌性化、杀雄作用，其中胞质不相容作用可以促进寄主的物种分化。对节肢动物Wolbachia感染情况的调研显示，膜翅目昆虫更易被Wolbachia感染，其中榕小蜂Wolbachia感染率更高，并且在不同榕小蜂物种间存在频繁的Wolbachia的水平传播。当Wolbachia与寄主线粒体单体型存在连锁不均衡关系时，寄主的线粒体多态性会发生一定改变，进而影响到线粒体DNA的系统发育研究的准确性。榕小蜂物种资源丰富，种间生态关系复杂，对榕小蜂类群内Wolbachia感染情况的深入调查，有助于我们理解Wolbachia水平传播的途径以及其与榕小蜂物种多样性的关系，进而更深入地理解榕树—榕小蜂—Wolbachia三者的相互作用与协同进化关系。
本文以功能性雌雄异株的木瓜榕上传粉榕小蜂Ceratosolen emarginatus、造瘿榕小蜂Apocryptophagus sp.和非传粉榕小蜂Philotrypesis sp.1、 Sycoscapter sp.1为研究材料，样品采集地点分布在海南省儋州榕园、鹦哥岭、黎母山、锦塘水库，以及云南省西双版纳植物园5个地点。经过标本采集——标本鉴定——DNA提取——基因扩增、测序——系统发育树构建——基因多样性分析，我们得到以下几个主要结果：
(1)通过对榕小蜂标本形态观察，我们初步确定了木瓜榕雌株上造瘿榕小蜂与雄株上造瘿榕小蜂在触角、前胸、翅、体色等部位有明显差异。通过分析cox1、ITS2基因，发现两者cox1序列分歧度达到80%，ITS2基因序列分歧度达到74.2%，而Bayes系统发育树分析则确定了雄株上造瘿榕小蜂和雌株上的造瘿榕小蜂为两个不同种，分别命名为Apocryptophagus sp.1和Apocryptophagus sp.2，并且两者既不是姐妹种，也不是隐存种。此外，引入化石榕小蜂Pegoscapus作为进化时间参照，构建cox1基因分子钟树，我们首次明确了两个造瘿榕小蜂都为新种，其中Apocryptophagus sp.2物种形成时间为520万年前，在榕小蜂体系中是一个较为年轻的榕小蜂物种。
(2)传粉榕小蜂Ceratosolen emarginatus和非传粉榕小蜂Sycoscapter sp.1、Philotrypesis sp.1的ITS2序列二级结构具有4个螺旋臂状结构的基本模型和相似的G+C含量，其中螺旋臂I区和IV区保守性较高，螺旋臂II区变异较大，通过在18S区和28S区自行设计特异引物，得到了这3种榕小蜂的ITS基因（ITS1+5.8S+ITS2）全长，有助于我们分析核基因核苷酸多样性特征。但是造瘿榕小蜂Apocryptophagus sp.2的ITS2转录产物二级结构不具备基本模型特征，螺旋臂状结构不稳定，G+C含量较高，干扰了榕小蜂ITS基因全长的扩增效果。因此，针对不同种类的榕小蜂，其核基因具有明显不同特征，种间差异较大，种内保守型较高，是一个高效的分子标记基因。
(3)所有研究对象中，苹果榕上非传粉榕小蜂Sycoscapter sp.1的mtDNA中性检测值为差异显著的负值结果，说明其cox1基因偏离了中性选择，群体大小变化分析，呈现多峰分布态势，排除了种群扩张的可能，该种群处于平衡状态，其他榕小蜂符合中性进化。
(4)木瓜榕和苹果榕上所有榕小蜂类群都感染了Wolbachia，且个体感染率为100%。Wolbachia株系鉴定：通过MLST法获得5个管家基因（gatB，coxA，hcpA，ftsZ和fbpA）以及wsp基因的等位片段值，我们在Profiles数据库得到了对应ST值，确定了榕小蜂感染的3种Wolbachia株系分别为wMel、wHa和A_NY_Calyp150744c。
(5)榕小蜂感染Wolbachia格局与mtDNA多样性的联系复杂多样：在造瘿榕小蜂Apocryptophagus sp.2种里，感染单一株系wMel个体显示mtDNA序列多样性较高，双重感染wMel和wHa株系个体的mtDNA序列多样性较低。但是，在造瘿榕小蜂Apocryptophagus sp.1种里，感染单一株系wMel个体的mtDNA序列多样性最高，感染另一种单一株系A_NY_Calyp150744c的mtDNA序列多样性最低，当发生这两个株系发生双重感染时，mtDNA序列多样性是居于中间的。不同榕小蜂物种感染株系情况不同，显示出不同mtDNA多样性特征。
(6) S-PLUS（R软件）分析所有造瘿榕小蜂总体模型，感染株系仅在不同地理位置间存在显著差异，与榕树雌果和雄果差异、榕小蜂性别差异无关。感染wMel株系在鹦哥岭和儋州、鹦哥岭和西双版纳以及鹦哥岭和锦塘两地间存在显著差异，其他株系以及株系多重感染并没有因为地理位置不同而出现相关性改变。
(7)通过对Wolbachia株系的研究，判断在木瓜榕上榕小蜂，Wolbachia的垂直传播和水平传播并存。株系wMel在榕小蜂种群内发生高效的垂直传播的同时，在种群间发生广泛的水平传播，而在苹果榕上非传粉榕小蜂Sycoscapter sp.1个体内只检测到株系wMel，传粉榕小蜂Ceratosolen emarginatus个体内却感染了wMel、 wHa和A_NY_Calyp150744c3种株系，很显然，虽然两者生态学联系密切，但是株系wHa和A_NY_Calyp150744c3还未在两个种间发生水平传播。
Figs (Moraceae: Ficus) and fig wasps (Insecta: Hymenoptera: Chaleidoidea) has beenknown as a classic example of co-evolution, and become the focus of researches on origin andevolution of mutualism, resource conflicts, the stabilization of mutualism, sex ratiodistribution. In this system, the complex fig wasps community, extreme sexual dimorphismand male polymorphism challenge fig wasps classification.In this thesis, we introduced aDNA barcoding technique. By sequencing the general standard cox1fragement, we can fastand accurate identification of fig wasps species.
Wolbachia symbionts are widespread intracellular bacteria that are found in arthropodsand nematodes. This maternally inherited endosymbiont could manipulate a lot ofreproductive processes in host, including incompatibility (cytoplasmic incompatibility),parthenogenesis, feminization, and male killing. It was proposed that CI may promote the hostspeciation. Several studies showed that hymenopteran more easy to infect Wolbachia,especially the higher infection rate in fig wasps and frequent horizontal transmission amongdifferent species. When Wolbachia and host mitochondrial haplotype exist linkagedisequilibrium, the host mitochondrial polymorphism should be changed, and then influencethe phylogeny based on mtDNA. The deeper research into the Wolbachia infection will helpus to learn more about Wolbachia transmission and the connection with diversity of species,and then more understanding the complex interaction and co-evolution of fig waspscommunity.
Here we studied the mtDNA polymorphism and Wolbachia infection of fig wasps onFicus auriculata and Ficus oligodon. Samples were collected from5different locations inDanzhou Campus, Hainan University, Yingge Mountain, Changjiang, Jin Tang and Xishuangbanna arboretum, Yunnan. Combining morphological identification with molecular markers,we found that the galler on the male syconia and the galler on the female syconia actually aredifferent species. And they are not sister species, with mtDNA divergence up to80%andITS2gene divergence up to74.26%. The gallers showed very higher mtDNA polymorphismfrom different locations. We also discussed the impact of geographical distribution on thecurrent programme of fig wasp taxonomy based on DNA barcoding. Additionally, through thecox1gene molecular clock time tree, we estimated that two Apocryptophagus gallers divergedabout5.2million years ago.
Alignment of ITS2sequences corrected by structural information showed that helixes Iand IV are the most conserved, whereas helix II is the most variable. The nucleotide composition (G+Ccontent) is similar among all species analyzed, except forApocryptophagus sp.2with instability secondary structure and higher G+C content. Furthermore, we also obtain the ITS gene (ITS1+5.8S+ITS2) from pollinating fig wasp Ceratosolenemarginatus and non-pollinating fig wasp Sycoscapter sp.1and Philotrypesis sp.1, showeddifferent gene type among different species, and conserved region in the same species, whichis a high-efficiency molecular marker.
Tajima’s D test suggest that the mtDNA molecular diversity of Sycoscapter sp.1onFicus oligodon deviating from the neutrality evolution. In addition，the population sizechanges analysis demonstrate multiple peak distribution, ruled out the possibility ofpopulation expansion. Other groups of fig wasps accord with the neutrality evolution.
Among all species analyzed, the Wolbachia infection is100%. Using MLST and wspgene, we obtained the ST from Profiles database, and confirmed3different strains: wMel、wHa and A_NY_Calyp150744c. The strains infection is also in connection with mtDNApolymorphism. For instance, the group mono-infected strain wMel of Apocryptophagus sp.2showed high mtDNA polymorphism. However, double-infected group showed low mtDNApolymorphism. In Apocryptophagus sp.1, the group mono-infected strain wMel showed thehighest mtDNA diversity, Obviously, the group mono-infected strain A_NY_Calyp150744cshowed the lowest mtDNA diversity. When double-infected, mtDNA polymorphism isintermediate.
The infection of all gallers species analyzed, even from different locations, had noconnection with the interaction among the gall/seed figs and female/male gallers. Theinfection of wMel strain showed significant divergence, such as YGL and DZ, YGL and BN,and the YGL and JT. However, the other strains and multiple infection did not showsignificant divergence on different geographic locations.
From the phylogenetic tree of the strains, we conjectured that there two transmissionmodels among fig wasps: strain wMel could high-efficiency vertical transfer and broadlyhorizontal transfer. On the contrary, in Ficus oligodon figs, the population of Sycoscapter sp.1just infected strain wMel; the population of Ceratosolen emarginatus infected all three strains,obviously, though the two fig wasp specis had closely ecological connection with each other,the horizontal transmission of the strains wHa and A_NY_Calyp150744c3had not yetoccurred.
本文以功能性雌雄异株的木瓜榕上传粉榕小蜂Ceratosolen emarginatus、造瘿榕小蜂Apocryptophagus sp.和非传粉榕小蜂Philotrypesis sp.1、 Sycoscapter sp.1为研究材料，样品采集地点分布在海南省儋州榕园、鹦哥岭、黎母山、锦塘水库，以及云南省西双版纳植物园5个地点。经过标本采集——标本鉴定——DNA提取——基因扩增、测序——系统发育树构建——基因多样性分析，我们得到以下几个主要结果：
(1)通过对榕小蜂标本形态观察，我们初步确定了木瓜榕雌株上造瘿榕小蜂与雄株上造瘿榕小蜂在触角、前胸、翅、体色等部位有明显差异。通过分析cox1、ITS2基因，发现两者cox1序列分歧度达到80%，ITS2基因序列分歧度达到74.2%，而Bayes系统发育树分析则确定了雄株上造瘿榕小蜂和雌株上的造瘿榕小蜂为两个不同种，分别命名为Apocryptophagus sp.1和Apocryptophagus sp.2，并且两者既不是姐妹种，也不是隐存种。此外，引入化石榕小蜂Pegoscapus作为进化时间参照，构建cox1基因分子钟树，我们首次明确了两个造瘿榕小蜂都为新种，其中Apocryptophagus sp.2物种形成时间为520万年前，在榕小蜂体系中是一个较为年轻的榕小蜂物种。
(2)传粉榕小蜂Ceratosolen emarginatus和非传粉榕小蜂Sycoscapter sp.1、Philotrypesis sp.1的ITS2序列二级结构具有4个螺旋臂状结构的基本模型和相似的G+C含量，其中螺旋臂I区和IV区保守性较高，螺旋臂II区变异较大，通过在18S区和28S区自行设计特异引物，得到了这3种榕小蜂的ITS基因（ITS1+5.8S+ITS2）全长，有助于我们分析核基因核苷酸多样性特征。但是造瘿榕小蜂Apocryptophagus sp.2的ITS2转录产物二级结构不具备基本模型特征，螺旋臂状结构不稳定，G+C含量较高，干扰了榕小蜂ITS基因全长的扩增效果。因此，针对不同种类的榕小蜂，其核基因具有明显不同特征，种间差异较大，种内保守型较高，是一个高效的分子标记基因。
(3)所有研究对象中，苹果榕上非传粉榕小蜂Sycoscapter sp.1的mtDNA中性检测值为差异显著的负值结果，说明其cox1基因偏离了中性选择，群体大小变化分析，呈现多峰分布态势，排除了种群扩张的可能，该种群处于平衡状态，其他榕小蜂符合中性进化。
(4)木瓜榕和苹果榕上所有榕小蜂类群都感染了Wolbachia，且个体感染率为100%。Wolbachia株系鉴定：通过MLST法获得5个管家基因（gatB，coxA，hcpA，ftsZ和fbpA）以及wsp基因的等位片段值，我们在Profiles数据库得到了对应ST值，确定了榕小蜂感染的3种Wolbachia株系分别为wMel、wHa和A_NY_Calyp150744c。
(5)榕小蜂感染Wolbachia格局与mtDNA多样性的联系复杂多样：在造瘿榕小蜂Apocryptophagus sp.2种里，感染单一株系wMel个体显示mtDNA序列多样性较高，双重感染wMel和wHa株系个体的mtDNA序列多样性较低。但是，在造瘿榕小蜂Apocryptophagus sp.1种里，感染单一株系wMel个体的mtDNA序列多样性最高，感染另一种单一株系A_NY_Calyp150744c的mtDNA序列多样性最低，当发生这两个株系发生双重感染时，mtDNA序列多样性是居于中间的。不同榕小蜂物种感染株系情况不同，显示出不同mtDNA多样性特征。
(6) S-PLUS（R软件）分析所有造瘿榕小蜂总体模型，感染株系仅在不同地理位置间存在显著差异，与榕树雌果和雄果差异、榕小蜂性别差异无关。感染wMel株系在鹦哥岭和儋州、鹦哥岭和西双版纳以及鹦哥岭和锦塘两地间存在显著差异，其他株系以及株系多重感染并没有因为地理位置不同而出现相关性改变。
(7)通过对Wolbachia株系的研究，判断在木瓜榕上榕小蜂，Wolbachia的垂直传播和水平传播并存。株系wMel在榕小蜂种群内发生高效的垂直传播的同时，在种群间发生广泛的水平传播，而在苹果榕上非传粉榕小蜂Sycoscapter sp.1个体内只检测到株系wMel，传粉榕小蜂Ceratosolen emarginatus个体内却感染了wMel、 wHa和A_NY_Calyp150744c3种株系，很显然，虽然两者生态学联系密切，但是株系wHa和A_NY_Calyp150744c3还未在两个种间发生水平传播。
Figs (Moraceae: Ficus) and fig wasps (Insecta: Hymenoptera: Chaleidoidea) has beenknown as a classic example of co-evolution, and become the focus of researches on origin andevolution of mutualism, resource conflicts, the stabilization of mutualism, sex ratiodistribution. In this system, the complex fig wasps community, extreme sexual dimorphismand male polymorphism challenge fig wasps classification.In this thesis, we introduced aDNA barcoding technique. By sequencing the general standard cox1fragement, we can fastand accurate identification of fig wasps species.
Wolbachia symbionts are widespread intracellular bacteria that are found in arthropodsand nematodes. This maternally inherited endosymbiont could manipulate a lot ofreproductive processes in host, including incompatibility (cytoplasmic incompatibility),parthenogenesis, feminization, and male killing. It was proposed that CI may promote the hostspeciation. Several studies showed that hymenopteran more easy to infect Wolbachia,especially the higher infection rate in fig wasps and frequent horizontal transmission amongdifferent species. When Wolbachia and host mitochondrial haplotype exist linkagedisequilibrium, the host mitochondrial polymorphism should be changed, and then influencethe phylogeny based on mtDNA. The deeper research into the Wolbachia infection will helpus to learn more about Wolbachia transmission and the connection with diversity of species,and then more understanding the complex interaction and co-evolution of fig waspscommunity.
Here we studied the mtDNA polymorphism and Wolbachia infection of fig wasps onFicus auriculata and Ficus oligodon. Samples were collected from5different locations inDanzhou Campus, Hainan University, Yingge Mountain, Changjiang, Jin Tang and Xishuangbanna arboretum, Yunnan. Combining morphological identification with molecular markers,we found that the galler on the male syconia and the galler on the female syconia actually aredifferent species. And they are not sister species, with mtDNA divergence up to80%andITS2gene divergence up to74.26%. The gallers showed very higher mtDNA polymorphismfrom different locations. We also discussed the impact of geographical distribution on thecurrent programme of fig wasp taxonomy based on DNA barcoding. Additionally, through thecox1gene molecular clock time tree, we estimated that two Apocryptophagus gallers divergedabout5.2million years ago.
Alignment of ITS2sequences corrected by structural information showed that helixes Iand IV are the most conserved, whereas helix II is the most variable. The nucleotide composition (G+Ccontent) is similar among all species analyzed, except forApocryptophagus sp.2with instability secondary structure and higher G+C content. Furthermore, we also obtain the ITS gene (ITS1+5.8S+ITS2) from pollinating fig wasp Ceratosolenemarginatus and non-pollinating fig wasp Sycoscapter sp.1and Philotrypesis sp.1, showeddifferent gene type among different species, and conserved region in the same species, whichis a high-efficiency molecular marker.
Tajima’s D test suggest that the mtDNA molecular diversity of Sycoscapter sp.1onFicus oligodon deviating from the neutrality evolution. In addition，the population sizechanges analysis demonstrate multiple peak distribution, ruled out the possibility ofpopulation expansion. Other groups of fig wasps accord with the neutrality evolution.
Among all species analyzed, the Wolbachia infection is100%. Using MLST and wspgene, we obtained the ST from Profiles database, and confirmed3different strains: wMel、wHa and A_NY_Calyp150744c. The strains infection is also in connection with mtDNApolymorphism. For instance, the group mono-infected strain wMel of Apocryptophagus sp.2showed high mtDNA polymorphism. However, double-infected group showed low mtDNApolymorphism. In Apocryptophagus sp.1, the group mono-infected strain wMel showed thehighest mtDNA diversity, Obviously, the group mono-infected strain A_NY_Calyp150744cshowed the lowest mtDNA diversity. When double-infected, mtDNA polymorphism isintermediate.
The infection of all gallers species analyzed, even from different locations, had noconnection with the interaction among the gall/seed figs and female/male gallers. Theinfection of wMel strain showed significant divergence, such as YGL and DZ, YGL and BN,and the YGL and JT. However, the other strains and multiple infection did not showsignificant divergence on different geographic locations.
From the phylogenetic tree of the strains, we conjectured that there two transmissionmodels among fig wasps: strain wMel could high-efficiency vertical transfer and broadlyhorizontal transfer. On the contrary, in Ficus oligodon figs, the population of Sycoscapter sp.1just infected strain wMel; the population of Ceratosolen emarginatus infected all three strains,obviously, though the two fig wasp specis had closely ecological connection with each other,the horizontal transmission of the strains wHa and A_NY_Calyp150744c3had not yetoccurred.
引文
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