膜翅目线粒体基因组的特征与进化及其在系统发育研究中的应用
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摘要
线粒体基因组具有基因组小、基因组成稳定、普遍为母性遗传和较少发生重组等特点,成为基因组学和进化研究的理想材料,也为系统发育等研究提供了丰富的分子标记。初步研究表明膜翅目线粒体基因组在碱基组成和基因排列等方面有其特殊性,然而相对于膜翅目庞大的类群,已测定的膜翅目线粒体基因组的种类非常有限。因此,对膜翅目线粒体基因组进行测序和分析,对揭示膜翅目线粒体基因组的进化以及研究该类群复杂的系统发育关系具有重要的意义。
本研究对膜翅目线粒体基因组进行了大规模测序和注释,利用比较基因组学和生物信息学等手段分析了膜翅目线粒体基因组的特征与进化,并通过大量的比较分析,阐明了相关的进化机制,在此基础上,基于线粒体全基因组序列对膜翅目在全变态类昆虫中的位置以及膜翅目内各类群的系统发育关系进行了研究。主要研究结果如下:
(1)首次测定了膜翅目5个科11个种和长翅目1个种的线粒体基因组序列,分别对每个基因组进行了注释,分析了各基因组的基因组成、基因间隔区、基因排列方式、密码子使用情况、tRNA和rRNA基因的二级结构以及A+T富含区的结构等;发现广旗腹蜂Evania appendigaster线粒体基因组中有一段位于atp8和atp6之间的基因间隔区并可以形成mRNA二级结构,推测该区域是蛋白质编码基因atp8和atp6转录产物切割的信号位点;发现了半闭弯尾姬蜂Diadegma semiclausum线粒体基因组中位于cox1和cox2之间A+T含量极高(99.1%)的一条串联重复序列(1515 bp),推测该区域是由于cox1基因3'末端一段17 bp序列发生滑连错配,并经过一系列独立的串联重复和随机突变、插入和缺失事件形成的;分析了白蜡吉丁虫柄腹茧蜂Spathius agrili、长尾全裂茧蜂Diachasmimorpha longicaudata和菜蛾盘绒茧蜂Cotesia vestalis A+T富含区中与复制/转录相关的元素(Poly-T stretch、[TA(A)]n-like stretch、颈环结构(Stem-and-loop Structure)和位于颈环结构5'端的ATA和3'端G(A)nT结构),首次在六足总纲中从结构上证明了A+T富含区颠倒的现象;发现菜蛾盘绒茧蜂线粒体基因组是目前已知基因重排最频繁的膜翅目线粒体基因组,推测认为其基因排列方式是由3类基因重排事件造成的。
(2)发现膜翅目线粒体基因组中发生重叠的基因很少发生基因重排,而发生重排的基因的两侧通常具有基因间隔区。在atp8和atp6之间以及nad4和nad4l之间通常具有一段基因重叠区,因而它们之间的相对位置较为稳定;发现一段位于trnS1和nad1之间的基因间隔区的保守序列,推测该区域为线粒体基因组复制终止的信号序列(mtTERM);膜翅目线粒体基因组中trnK和trnS2使用与其它线粒体基因组不同的TTT和TCT做反密码子,发现这两个tRNA基因中非常规反密码子的使用与基因重排具有较高的相关性。
(3)通过分析未校正的Pi、非同义替换率与同义替换率的比率Ka/Ks以及Jukes-Cantor校正的非同义替换率与同义替换率的比率Ka/Ks(JC)等进化参数,发现膜翅目线粒体基因进化的速率高于其它全变态类昆虫;在全变态类昆虫中,had6、atp8、nad4l和nad2的进化速率最快,cox1、cox2、cob和had5基因较保守;膜翅目中,意大利蜜蜂Apis mellifera、中国红光熊蜂Bombus ingitus、双色麦峰Melipogla bicolor、盖拉头甲肿腿蜂Cephalonomia gallicola、眼斑驼盾蚁蜂Radoszkowskius oculata和樟虫长体茧蜂Macrocentrus camphoraphilus的Ka/Ks较高,长尾全裂茧蜂、金小蜂Nasonia longicornis和叶蜂Perga condei的较低。茧蜂科Braconidae内部各亚科的种类之间Ka/Ks差异较大。多数膜翅目线粒体基因组中发生颠换的次数多于转换。广旗腹蜂和眼斑驼盾蚁蜂发生替换(转换+颠换)的次数最多。
(4)膜翅目线粒体基因具有较高的重排速率,基因重排的程度在膜翅目各类群间存在差异,广腰亚目基因排列较细腰亚目保守,叶蜂P.condei已测序列中只发生了1次基因重排事件,而细腰亚目中各种类的基因重排次数在2～18不等;发生重排的基因主要集中在4个重排热点区:A+T富含区-nad2、nad2-cox1、cox2-atp8和nad3-nad5;重排的基因以tRNA为主,蛋白质编码基因和rRNA基因的重排只发生在少数种类中;在膜翅目线粒体基因组中,移位、倒置、基因洗牌和异位倒置等不同类型的重排事件发生的频率相似;首次提出了异位倒置是由两次重排事件引起的重排机理。
(5)在目前已测的六足总纲各目中,膜翅目线粒体基因组的A+T含量最高,鳞翅目Lepidoptera次之,缨翅目Thysanoptera和等翅目Isoptera的最低。膜翅目中,广腰亚目线粒体基因组的A+T含量较细腰亚目低;但在细腰亚目中,旗腹蜂的A+T含量较低,甚至低于广腰亚目中的种类。
(6)膜翅目中茧蜂科昆虫线粒体基因组的碱基组成偏向性发生了颠倒,其A+T富含区与复制/转录相关的元素的颠倒支持了碱基组成偏向性的颠倒是由于基因组复制起点的倒置引起的理论假设。
(7)比较分析了133个昆虫的线粒体基因组,发现碱基组成偏向性的颠倒在六足总纲中独立进化了3次,分别出现在膜翅目Hymenoptera茧蜂科Braconidae(7个种)、虱目Phthiraptera长角羽虱科Philopteridae(2个种)和半翅目Hemiptera粉虱科Aleyrodidae(6个种);单个基因上的A+T偏斜的正负与基因的方向相关,而GC偏斜的正负与基因组复制起点的方向相关;结合最新的复制和转录研究理论,提出了一个新的关于碱基组成偏向性产生的假说:“不对称性脱氨基化假说(Asymmetric DeaminationHypothesis)”,即复制过程中A脱氨基化多于转录过程,转录过程C脱氨基化多于复制过程。
(8)利用线粒体全基因组序列对全变态类昆虫的系统发育关系进行了研究,结果支持膜翅目处于全变态类昆虫的基部位置,以及脉翅类Neuropterida(脉翅目Neuroptera+广翅目Megaloptera)的存在及其与“长翅目Mecoptera+双翅目Diptera”的姐妹群关系;对膜翅目内部各大类群的分析表明细蜂总科Proctotrupidea和小蜂总科Chalcidoidea以及姬蜂总科Ichneumonoidea和针尾部Aculeata(蜜蜂总科Apoidea+(蜾蠃科Eumenidae+胡蜂科Vespidae))为姐妹群关系;在加入旗腹蜂科Evaniidae、肿腿蜂科Bethylidae和蚁蜂科Mutillidae进行分析时,得到了“姬蜂总科+(旗腹蜂科+((肿腿蜂科+蚁蜂科)+(蜜蜂总科Apoidea+(蜾蠃科+胡蜂科))))”的系统发育关系,支持针尾部的单系性,旗腹蜂科与针尾部的姐妹群关系,姬蜂总科与(旗腹蜂科+针尾部)的姐妹群关系,但发现肿腿蜂科和蚁蜂科为姐妹群关系,表明胡蜂总科Vespoidea(蜾蠃科,胡蜂科,蚁蜂科)是一个并系群;对茧蜂科Braconidae的系统发育关系分析表明蚜茧蜂亚科Aphidiinae与“圆口类Cyclostomes”为姐妹群关系,小腹茧蜂亚科群Microgastroids与长茧蜂科亚科群Helconoids构成“非圆口类Noncyclostomes”并与“蚜茧蜂亚科+圆口类”构成姐妹群关系。
Metazoan mitochondrial genome is usually used for determining population structure. phylogenetic relationships and general evolutionary events because of its small genome size, stable gene content,uniparental inheritance,lack of extensive recombination and the accelerated rate of nucleotide substitution.Previous studies indicated that there are a lot of special characters in hymenopteran mitochondrial genomes,such as high A+T content and frequent gene rearrangement.However,limited mitochondrial genomes,representing only a few families in this species-rich insect order,have been sequenced.Therefore,characterization of more hymenopteran mitochondrial genomes is needed to address evolutionary questions and traits,and to revole phylogenetic relationships of this group.
In this study,we conducted a large scale sequencing and annotation of hymenopteran mitochondrial genomes,and comparied them with other sequenced mitochondrial genomes in Hexapoda.especially in Hymenoptera.to explore the evolutionary traits and mechanisms in mitochondrial genomes.Additionally,we assessed the utility of complete mitochondrial genome sequences as markers for phylogenetic analyses of Hymenoptera and Holometabola. Consequently we concluded eight main points as follows:
(1) Eleven mitochondrial genomes representing five hymenopteran families and one mitochondrial genome representing Mecoptera(Hexapoda:Holometabola) were sequenced and annotated for the first time.Gene content,intergenic region,gene arrangement,codon usage,tRNA and rRNA secondary structures as well as characters of A+T-rich region were analyzed in each sequenced mitochondrial genome.A large intergenic region was found between atp8 and atp6 in Evania appendigasrer,which could form an mRNA secondary structure and therefore was supposed to facilitate cleavage between these abutting proteins transcript.An extremely A+T-riched(99.1%) 1515 bp tandem repeat region with three types of repeat elements was located between cox1 and cox2 in Diadegma semiclausum,and the most likely ancestral element originated from the 3' end of cox1.The formation of this region was proposed to be independent tandem duplications followed by mutation/insertion/deletion.The inversion of A+T-rich region in Hexapoda was evidenced structurally for the first time due to its exsistence in Diachasmimorpha longicaudata,Spathius agrili and Cotesia vestalis mitochondrial genomes.The most extensive rearrangement events in Hymenoptera were found in Cotesia vestalis mitochondrial genome,including seven protein-coding and 11 tRNA genes.
(2) Overlapping genes were rarely rearranged,while those rearranged genes usually have intergenetic regions inbetween.A conserved motif was found between trns1 and nad1.which was supposed to be associated with the termination of genome transcription(mtTERM).trnS2 and trnK usually use abnormal anticodon TCT and TTT respectively,which were probably related to gene rearrangement.
(3) The values of uncorrected nucleotide diversity(Pi),ratio of the rate of non-synonymous substitutions to the rate of synonymous substitutions(Ka/Ks) and Jukes-Cantor corrected Ka/Ks indicated that mitochondrial genomes evolved faster in Hymenoptera than in other holometabolous orders.For individual genes in holometabolous mitochondrial genomes,nad6,atp8 and nad4l evolved the fastest while cox1,cox2,cob and nad5 evolved much slowly.In Hymenoptera,Apis mellifera,Bombus ingitus,Melipona bicolor,Cephalonomia gallicola,Radoszkowskius oculata and Macrocentrus camphoraphilus had a high Ka/Ks value,while D.longicaudata,Nasonia longicornis and Perga condei had a low Ka/Ks value.The values of Ka/Ks are variable among species of different subfamilies in the famliy Braconidae.Most species had more transitions than transversions in Hymenoptera. Evania appendigaster and R.oculata had more substitutions than other species.
(4) In Hymenopteran mitochondrial genomes,gene arrangement is conserved in the basal suborder,Symphyta,while frequent gene rearrangements are observed in the other suborder, Apocrita.Gene rearrangements mainly occurred in four hot spots,i.e.A+T-rich region-nad2, nad2-cox1,cox2-atp8 and nad3-nad5.Most rearranged genes are tRNAs,but only a few protein-coding or rRNA genes were rearranged.Translocation,inversion,shuffling and remote inversion events were found to be present in nearly equal frequency.The remote inversion was supposed to be caused by two independent recombination events.
(5) The hymenopteran mitochondrial genomes had the highest A+T content in Holometabola,followed by Lepidoptera,while the Thysanoptera and Isoptera had the lowest one.A+T content is usually higher in Apocrita than in Symphyta except for E.appendigaster, which even had a lower A+T content than P.condei,a species of Symphyta.
(6) In all braconid species,strand asymmetry was reversed,which supported the hypothesis that reversal of strand asymmetry is caused by inversion of replication/transcriotion -related A+T-rich region.
(7) A broad survey of strand asymmetry among 133 sequenced hexapod mitochondrial genomes showed that reversal of strand asymmetry evolved triple in Hexapoda,as here in Braconidae and other two families,Philopteridae(Phthiraptera) and Aleyrodidae(Hemiptera). The sign of AT skew on individual gene is associated with gene direction while GC skew is associated with replication orientation.Accordingly,we proposed a new hypothesis of "Asymmetric deamination" for strand asymmetry,that is.more C deaminations during transcription than replication whereas more A deamination during replication than transcription.
(8) Phylogenetic analyses show that complete mitochondrial genome sequences could recover the documented basal position of Hymenoptera among holometabolous orders.The sister-group relationship between Neuropterida(Neuroptera+Megaloptera in this study) and "Mecoptera+Diptera" was resolved.The clade Proctotrupomorpha (Proctotrupoidea+Chalcidoidea in this study) and the sister-group relationship between Ichneumonoidea and Aculeata were supported within Hymenoptera.When the families of Evaniidae,Bethylidae,Mutillidae are included in analyses,the supported relationship in hymenopteran lineage is "Ichneumonoidea+(Evaniidae+((Bethylidae+Bethylidae)+(Apoidea+ (Eumenidae+Vespoidea))))",indicating that Evaniidae is a sister group of Aculeata. lchneumonoidea a sister of"Evaniidae+Aculeata",and Vespoidea a paraphyletic group.In Braconidae.Aphidiinae is sister to Cyclostomes,Microgastroids and Helconoids form the clade Noncyclostomes.and a relationship of"(Aphidiinae+Cyclostomes)+Noncyclostomes" was supported.
本研究对膜翅目线粒体基因组进行了大规模测序和注释,利用比较基因组学和生物信息学等手段分析了膜翅目线粒体基因组的特征与进化,并通过大量的比较分析,阐明了相关的进化机制,在此基础上,基于线粒体全基因组序列对膜翅目在全变态类昆虫中的位置以及膜翅目内各类群的系统发育关系进行了研究。主要研究结果如下:
(1)首次测定了膜翅目5个科11个种和长翅目1个种的线粒体基因组序列,分别对每个基因组进行了注释,分析了各基因组的基因组成、基因间隔区、基因排列方式、密码子使用情况、tRNA和rRNA基因的二级结构以及A+T富含区的结构等;发现广旗腹蜂Evania appendigaster线粒体基因组中有一段位于atp8和atp6之间的基因间隔区并可以形成mRNA二级结构,推测该区域是蛋白质编码基因atp8和atp6转录产物切割的信号位点;发现了半闭弯尾姬蜂Diadegma semiclausum线粒体基因组中位于cox1和cox2之间A+T含量极高(99.1%)的一条串联重复序列(1515 bp),推测该区域是由于cox1基因3'末端一段17 bp序列发生滑连错配,并经过一系列独立的串联重复和随机突变、插入和缺失事件形成的;分析了白蜡吉丁虫柄腹茧蜂Spathius agrili、长尾全裂茧蜂Diachasmimorpha longicaudata和菜蛾盘绒茧蜂Cotesia vestalis A+T富含区中与复制/转录相关的元素(Poly-T stretch、[TA(A)]n-like stretch、颈环结构(Stem-and-loop Structure)和位于颈环结构5'端的ATA和3'端G(A)nT结构),首次在六足总纲中从结构上证明了A+T富含区颠倒的现象;发现菜蛾盘绒茧蜂线粒体基因组是目前已知基因重排最频繁的膜翅目线粒体基因组,推测认为其基因排列方式是由3类基因重排事件造成的。
(2)发现膜翅目线粒体基因组中发生重叠的基因很少发生基因重排,而发生重排的基因的两侧通常具有基因间隔区。在atp8和atp6之间以及nad4和nad4l之间通常具有一段基因重叠区,因而它们之间的相对位置较为稳定;发现一段位于trnS1和nad1之间的基因间隔区的保守序列,推测该区域为线粒体基因组复制终止的信号序列(mtTERM);膜翅目线粒体基因组中trnK和trnS2使用与其它线粒体基因组不同的TTT和TCT做反密码子,发现这两个tRNA基因中非常规反密码子的使用与基因重排具有较高的相关性。
(3)通过分析未校正的Pi、非同义替换率与同义替换率的比率Ka/Ks以及Jukes-Cantor校正的非同义替换率与同义替换率的比率Ka/Ks(JC)等进化参数,发现膜翅目线粒体基因进化的速率高于其它全变态类昆虫;在全变态类昆虫中,had6、atp8、nad4l和nad2的进化速率最快,cox1、cox2、cob和had5基因较保守;膜翅目中,意大利蜜蜂Apis mellifera、中国红光熊蜂Bombus ingitus、双色麦峰Melipogla bicolor、盖拉头甲肿腿蜂Cephalonomia gallicola、眼斑驼盾蚁蜂Radoszkowskius oculata和樟虫长体茧蜂Macrocentrus camphoraphilus的Ka/Ks较高,长尾全裂茧蜂、金小蜂Nasonia longicornis和叶蜂Perga condei的较低。茧蜂科Braconidae内部各亚科的种类之间Ka/Ks差异较大。多数膜翅目线粒体基因组中发生颠换的次数多于转换。广旗腹蜂和眼斑驼盾蚁蜂发生替换(转换+颠换)的次数最多。
(4)膜翅目线粒体基因具有较高的重排速率,基因重排的程度在膜翅目各类群间存在差异,广腰亚目基因排列较细腰亚目保守,叶蜂P.condei已测序列中只发生了1次基因重排事件,而细腰亚目中各种类的基因重排次数在2～18不等;发生重排的基因主要集中在4个重排热点区:A+T富含区-nad2、nad2-cox1、cox2-atp8和nad3-nad5;重排的基因以tRNA为主,蛋白质编码基因和rRNA基因的重排只发生在少数种类中;在膜翅目线粒体基因组中,移位、倒置、基因洗牌和异位倒置等不同类型的重排事件发生的频率相似;首次提出了异位倒置是由两次重排事件引起的重排机理。
(5)在目前已测的六足总纲各目中,膜翅目线粒体基因组的A+T含量最高,鳞翅目Lepidoptera次之,缨翅目Thysanoptera和等翅目Isoptera的最低。膜翅目中,广腰亚目线粒体基因组的A+T含量较细腰亚目低;但在细腰亚目中,旗腹蜂的A+T含量较低,甚至低于广腰亚目中的种类。
(6)膜翅目中茧蜂科昆虫线粒体基因组的碱基组成偏向性发生了颠倒,其A+T富含区与复制/转录相关的元素的颠倒支持了碱基组成偏向性的颠倒是由于基因组复制起点的倒置引起的理论假设。
(7)比较分析了133个昆虫的线粒体基因组,发现碱基组成偏向性的颠倒在六足总纲中独立进化了3次,分别出现在膜翅目Hymenoptera茧蜂科Braconidae(7个种)、虱目Phthiraptera长角羽虱科Philopteridae(2个种)和半翅目Hemiptera粉虱科Aleyrodidae(6个种);单个基因上的A+T偏斜的正负与基因的方向相关,而GC偏斜的正负与基因组复制起点的方向相关;结合最新的复制和转录研究理论,提出了一个新的关于碱基组成偏向性产生的假说:“不对称性脱氨基化假说(Asymmetric DeaminationHypothesis)”,即复制过程中A脱氨基化多于转录过程,转录过程C脱氨基化多于复制过程。
(8)利用线粒体全基因组序列对全变态类昆虫的系统发育关系进行了研究,结果支持膜翅目处于全变态类昆虫的基部位置,以及脉翅类Neuropterida(脉翅目Neuroptera+广翅目Megaloptera)的存在及其与“长翅目Mecoptera+双翅目Diptera”的姐妹群关系;对膜翅目内部各大类群的分析表明细蜂总科Proctotrupidea和小蜂总科Chalcidoidea以及姬蜂总科Ichneumonoidea和针尾部Aculeata(蜜蜂总科Apoidea+(蜾蠃科Eumenidae+胡蜂科Vespidae))为姐妹群关系;在加入旗腹蜂科Evaniidae、肿腿蜂科Bethylidae和蚁蜂科Mutillidae进行分析时,得到了“姬蜂总科+(旗腹蜂科+((肿腿蜂科+蚁蜂科)+(蜜蜂总科Apoidea+(蜾蠃科+胡蜂科))))”的系统发育关系,支持针尾部的单系性,旗腹蜂科与针尾部的姐妹群关系,姬蜂总科与(旗腹蜂科+针尾部)的姐妹群关系,但发现肿腿蜂科和蚁蜂科为姐妹群关系,表明胡蜂总科Vespoidea(蜾蠃科,胡蜂科,蚁蜂科)是一个并系群;对茧蜂科Braconidae的系统发育关系分析表明蚜茧蜂亚科Aphidiinae与“圆口类Cyclostomes”为姐妹群关系,小腹茧蜂亚科群Microgastroids与长茧蜂科亚科群Helconoids构成“非圆口类Noncyclostomes”并与“蚜茧蜂亚科+圆口类”构成姐妹群关系。
Metazoan mitochondrial genome is usually used for determining population structure. phylogenetic relationships and general evolutionary events because of its small genome size, stable gene content,uniparental inheritance,lack of extensive recombination and the accelerated rate of nucleotide substitution.Previous studies indicated that there are a lot of special characters in hymenopteran mitochondrial genomes,such as high A+T content and frequent gene rearrangement.However,limited mitochondrial genomes,representing only a few families in this species-rich insect order,have been sequenced.Therefore,characterization of more hymenopteran mitochondrial genomes is needed to address evolutionary questions and traits,and to revole phylogenetic relationships of this group.
In this study,we conducted a large scale sequencing and annotation of hymenopteran mitochondrial genomes,and comparied them with other sequenced mitochondrial genomes in Hexapoda.especially in Hymenoptera.to explore the evolutionary traits and mechanisms in mitochondrial genomes.Additionally,we assessed the utility of complete mitochondrial genome sequences as markers for phylogenetic analyses of Hymenoptera and Holometabola. Consequently we concluded eight main points as follows:
(1) Eleven mitochondrial genomes representing five hymenopteran families and one mitochondrial genome representing Mecoptera(Hexapoda:Holometabola) were sequenced and annotated for the first time.Gene content,intergenic region,gene arrangement,codon usage,tRNA and rRNA secondary structures as well as characters of A+T-rich region were analyzed in each sequenced mitochondrial genome.A large intergenic region was found between atp8 and atp6 in Evania appendigasrer,which could form an mRNA secondary structure and therefore was supposed to facilitate cleavage between these abutting proteins transcript.An extremely A+T-riched(99.1%) 1515 bp tandem repeat region with three types of repeat elements was located between cox1 and cox2 in Diadegma semiclausum,and the most likely ancestral element originated from the 3' end of cox1.The formation of this region was proposed to be independent tandem duplications followed by mutation/insertion/deletion.The inversion of A+T-rich region in Hexapoda was evidenced structurally for the first time due to its exsistence in Diachasmimorpha longicaudata,Spathius agrili and Cotesia vestalis mitochondrial genomes.The most extensive rearrangement events in Hymenoptera were found in Cotesia vestalis mitochondrial genome,including seven protein-coding and 11 tRNA genes.
(2) Overlapping genes were rarely rearranged,while those rearranged genes usually have intergenetic regions inbetween.A conserved motif was found between trns1 and nad1.which was supposed to be associated with the termination of genome transcription(mtTERM).trnS2 and trnK usually use abnormal anticodon TCT and TTT respectively,which were probably related to gene rearrangement.
(3) The values of uncorrected nucleotide diversity(Pi),ratio of the rate of non-synonymous substitutions to the rate of synonymous substitutions(Ka/Ks) and Jukes-Cantor corrected Ka/Ks indicated that mitochondrial genomes evolved faster in Hymenoptera than in other holometabolous orders.For individual genes in holometabolous mitochondrial genomes,nad6,atp8 and nad4l evolved the fastest while cox1,cox2,cob and nad5 evolved much slowly.In Hymenoptera,Apis mellifera,Bombus ingitus,Melipona bicolor,Cephalonomia gallicola,Radoszkowskius oculata and Macrocentrus camphoraphilus had a high Ka/Ks value,while D.longicaudata,Nasonia longicornis and Perga condei had a low Ka/Ks value.The values of Ka/Ks are variable among species of different subfamilies in the famliy Braconidae.Most species had more transitions than transversions in Hymenoptera. Evania appendigaster and R.oculata had more substitutions than other species.
(4) In Hymenopteran mitochondrial genomes,gene arrangement is conserved in the basal suborder,Symphyta,while frequent gene rearrangements are observed in the other suborder, Apocrita.Gene rearrangements mainly occurred in four hot spots,i.e.A+T-rich region-nad2, nad2-cox1,cox2-atp8 and nad3-nad5.Most rearranged genes are tRNAs,but only a few protein-coding or rRNA genes were rearranged.Translocation,inversion,shuffling and remote inversion events were found to be present in nearly equal frequency.The remote inversion was supposed to be caused by two independent recombination events.
(5) The hymenopteran mitochondrial genomes had the highest A+T content in Holometabola,followed by Lepidoptera,while the Thysanoptera and Isoptera had the lowest one.A+T content is usually higher in Apocrita than in Symphyta except for E.appendigaster, which even had a lower A+T content than P.condei,a species of Symphyta.
(6) In all braconid species,strand asymmetry was reversed,which supported the hypothesis that reversal of strand asymmetry is caused by inversion of replication/transcriotion -related A+T-rich region.
(7) A broad survey of strand asymmetry among 133 sequenced hexapod mitochondrial genomes showed that reversal of strand asymmetry evolved triple in Hexapoda,as here in Braconidae and other two families,Philopteridae(Phthiraptera) and Aleyrodidae(Hemiptera). The sign of AT skew on individual gene is associated with gene direction while GC skew is associated with replication orientation.Accordingly,we proposed a new hypothesis of "Asymmetric deamination" for strand asymmetry,that is.more C deaminations during transcription than replication whereas more A deamination during replication than transcription.
(8) Phylogenetic analyses show that complete mitochondrial genome sequences could recover the documented basal position of Hymenoptera among holometabolous orders.The sister-group relationship between Neuropterida(Neuroptera+Megaloptera in this study) and "Mecoptera+Diptera" was resolved.The clade Proctotrupomorpha (Proctotrupoidea+Chalcidoidea in this study) and the sister-group relationship between Ichneumonoidea and Aculeata were supported within Hymenoptera.When the families of Evaniidae,Bethylidae,Mutillidae are included in analyses,the supported relationship in hymenopteran lineage is "Ichneumonoidea+(Evaniidae+((Bethylidae+Bethylidae)+(Apoidea+ (Eumenidae+Vespoidea))))",indicating that Evaniidae is a sister group of Aculeata. lchneumonoidea a sister of"Evaniidae+Aculeata",and Vespoidea a paraphyletic group.In Braconidae.Aphidiinae is sister to Cyclostomes,Microgastroids and Helconoids form the clade Noncyclostomes.and a relationship of"(Aphidiinae+Cyclostomes)+Noncyclostomes" was supported.
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