蝎蛉科昆虫胚胎发育研究（长翅目）
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摘要
长翅目Mecoptera是全变态类昆虫中唯一在幼虫期具复眼的昆虫类群，反映出长翅目可能是全变态类昆虫最基部的分支，是联系全变态类与不全变态类昆虫的重要纽带，因此在昆虫纲（尤其是全变态类昆虫）系统发育研究中占据重要地位。深入研究长翅目胚胎发育过程中的器官发生特征以及附肢同源性关系，有望从形态发生和起源角度来探讨全变态类昆虫的进化和系统发育问题，在整个昆虫纲中具有重要意义。
本文以长翅目蝎蛉科Panorpidae昆虫为代表，利用光镜以及电子显微镜技术，采用比较胚胎学、组织学和超微结构等方法，对蝎蛉科昆虫的胚胎发育过程进行了详细研究，特别是针对争议已久的上颚与下颚的同源关系、器官起源问题(包括胚膜、消化道以及神经系统等)、胸足与腹足的同源性等问题进行了深入的探讨。在此基础上，结合扁蚊蝎蛉（长翅目）与其他蠋式幼虫代表种粘虫Leucania separata（鳞翅目）和麦叶蜂Dolerustritici（膜翅目）的腹部附肢发育情况，分析了蠋式幼虫的腹足发育模式，探讨不同昆虫类群腹足的起源与进化，并进一步揭示其同源关系，为全变态类昆虫的系统发育和进化研究提供更多的依据。主要研究结果如下：
蝎蛉的上颚基部在发育初期有不明显的分节，中期分节明显，随着上颚的发育以及臼齿叶和切齿叶的分化，上颚基部分节逐渐消失。根据其分节情况，我们支持上颚由两部分组成的观点，即基部较小的上颚亚基节和端部较长的上颚基节。上颚基部退化的亚基节与下颚轴节同源，臼齿叶和切齿叶为基内叶，分别与下颚的内颚叶和外颚叶具有系列同源关系。
研究发现，太白蝎蛉Panorpa obtusa的口道和肛道由外胚层内陷发育而来，二者同时出现在胚胎的头中部和腹部末端表层；6根马氏管起源于肛道前端两侧的外胚层突起；中肠是由胚胎两端相向生长的内胚层细胞带发育而来。相向的两对细胞带结合并伸展，包裹卵黄并最终形成中肠原基；神经节细胞由成神经细胞发育而来，在神经节、神经纤维和侧神经索的形成中起到主要作用。
通过对大蝎蛉Dicerapanorpa magna胸、腹节附肢发育过程的研究，我们发现位于胸节两侧的胸足原基，最终发育为5节的胸足，包括基节、腿节、胫节、跗节和前跗节。与胸足相比，腹足原基出现在腹部内侧靠近腹中线的位置，与胸足着生位置一致的真正的腹部附肢原基在胚胎发育过程中消失，仅在腹侧留下三角形的退化痕迹。
而其他蠋式幼虫（粘虫和麦叶蜂）的腹足为原生构造，直接由腹足原基发育而来，其中粘虫在胚胎期与胸足原基着生位置相同，而麦叶蜂则与蝎蛉相似，其腹足的着生位置更靠近内侧的腹中线。粘虫和麦叶蜂的腹足原基最终发育形成发达的腹足，作为重要的运动器官。与之相比，长翅目蝎蛉科和蚊蝎蛉科幼虫短小的腹足基本无行动功能，很可能是为保护腹部腹面而衍生出的次生适应性构造。
由此我们认为，蝎蛉腹足并非真正的腹部附肢，腹足与胸足也并非为系列同源；而其他蠋式幼虫的腹足无论是从起源还是从功能和形态上都各不相同，因此其腹足并不具同源关系，极有可能是独立演化而来。根据腹足的不同起源，我们对蠋式幼虫的概念进行了初步修订，认为蠋式幼虫应分为原生型和次生型两种。
Mecoptera is one of the most primitive orders in holometabolous insects because theybear a pair of prominent compound eyes in the larval stage, representing the intermediate linkbetween the Holometabola and Hemimetabola and occupying an important position inphylogenetic study of insect (especially in Holometabola). Study on the organogeneticfeatures and appendage homology in Mecoptera embryogenesis can help explore thephylogenetics and evolution of the holometabolous insects based on both morphogensis andevolutionary aspects.
Based on the comparative embryology, histology and ultrastructural methods, we usedlight and electronic microscopy techniques to study the embryonic development ofPanorpidae in detail, in attempt to solve some long-standing controversial problems, such asthe homology between mandibles and maxillia, organogenesis (including embryonicmembrane, the alimentary canal, and nervous system), and the homology of thorax legs andprolegs. Combining with the abdominal appendages in representative species of othereruciform larvae Leucania separate (Lepidoptera) and Dolerus tritici (Hymenoptera), as wellas Bittacus planus (Mecoptera), we analyzed the developmental models of eruciform larvae,explored the origin and evolution of prolegs in different insect groups, and further revealedtheir homology. Our study may provide more evidences for the phylogenetic and evolutionarystudies of the holometabolous insects. The main results are as follows:
The segmentation on the mandible of Panorpidae is unconspicuous in early stage anddistinct in middle stage of the embryonic development. As the development of mandibles anddifferentiation of the molar lobe and incisor lobe, the basal segment of the mandible isgradually disappeared. Based on the segmentation, we considered that the mandible consistsof two parts, the smaller basal mandibular subcoxa and longer distal mandibular coxa. Thereduced mandibular subcoxa is homologous with the cardo of maxilla. The molar and incisorlobes are endites, serially homologous with the lacinia and galea of maxilla, respectively.
The results show that the invaginations of stomatodeum and proctodeum of Panorpobtusa are formed by the ectoderm, simultaneously occurring at the surface of embryonichead center and the end of abdominal segment. Six Malpighian tubules are derived from theectodermal processes at the end of lateral proctodaeum wall. The midgut originates from the endodermal cell bands, which are situated at the anterior and posterior embryo. Two pairedcell bands in both directions combine together and extend towards each other, finally enclosethe yolks and form the midgut rudiment. The ganglion cells formed by the neuroblast take animportant role in ganglion, nerve fiber, and lateral nerve cord formations.
During the investigation of the thoracic and abdominal appendage development ofDicerapanorpa magna, we found that the thoracic leg rudiments are located at the lateralsides in each segment and finally develop as the five-segmented thoracic legs, including coxa,femur, tibia, tarsus, and pretarsus. Compared with the thoracic legs, the proleg primordia aresituated at the inner side near the midventral line of the abdomen. The primary true abdominalappendages along the same line of the thoracic legs are disappeared gradually duringembryogenesis, only leaving flat vestiges on the lateral sides of the abdomen.
However, the prolegs in other eruciform larvae (Leucania separate and Dolerus tritici)are primary structures, which are developed from the proleg rudiment directly. The prolegprimordia of L. separate are located along the same line of the thoracic leg rudiments.However, the positions of the proleg primordia in both D. tritici and Panorpa obtusa aremuch closer to the inner midventral line of the abdomen. The proleg primordia of L. separateand D. tritici finally developed into stout prolegs as the important locomotion organs, whereasthe prolegs of Panorpidae and Bittacidae (Mecoptera) larvae are small and short,fundamentally no locomotory functions. The incompletely degenerated prolegs are very likelyto function as protecting the abdomen.
Hence we speculate that the prolegs of panorpids are not the true abdominal appendages.The abdominal prolegs and thoracic legs are not serially homologous. Compared with that ofMecoptera, the prolegs of other eruciform larvae are distinct in origin, function or morphology.Therefore, the prolegs are not homologous, but very likely evolve independently. Accordingto the distinct origin of the prolegs, we modified the concept of eruciform larvae temporarilyas that they can be subdivided into primitive and secondary types.
本文以长翅目蝎蛉科Panorpidae昆虫为代表，利用光镜以及电子显微镜技术，采用比较胚胎学、组织学和超微结构等方法，对蝎蛉科昆虫的胚胎发育过程进行了详细研究，特别是针对争议已久的上颚与下颚的同源关系、器官起源问题(包括胚膜、消化道以及神经系统等)、胸足与腹足的同源性等问题进行了深入的探讨。在此基础上，结合扁蚊蝎蛉（长翅目）与其他蠋式幼虫代表种粘虫Leucania separata（鳞翅目）和麦叶蜂Dolerustritici（膜翅目）的腹部附肢发育情况，分析了蠋式幼虫的腹足发育模式，探讨不同昆虫类群腹足的起源与进化，并进一步揭示其同源关系，为全变态类昆虫的系统发育和进化研究提供更多的依据。主要研究结果如下：
蝎蛉的上颚基部在发育初期有不明显的分节，中期分节明显，随着上颚的发育以及臼齿叶和切齿叶的分化，上颚基部分节逐渐消失。根据其分节情况，我们支持上颚由两部分组成的观点，即基部较小的上颚亚基节和端部较长的上颚基节。上颚基部退化的亚基节与下颚轴节同源，臼齿叶和切齿叶为基内叶，分别与下颚的内颚叶和外颚叶具有系列同源关系。
研究发现，太白蝎蛉Panorpa obtusa的口道和肛道由外胚层内陷发育而来，二者同时出现在胚胎的头中部和腹部末端表层；6根马氏管起源于肛道前端两侧的外胚层突起；中肠是由胚胎两端相向生长的内胚层细胞带发育而来。相向的两对细胞带结合并伸展，包裹卵黄并最终形成中肠原基；神经节细胞由成神经细胞发育而来，在神经节、神经纤维和侧神经索的形成中起到主要作用。
通过对大蝎蛉Dicerapanorpa magna胸、腹节附肢发育过程的研究，我们发现位于胸节两侧的胸足原基，最终发育为5节的胸足，包括基节、腿节、胫节、跗节和前跗节。与胸足相比，腹足原基出现在腹部内侧靠近腹中线的位置，与胸足着生位置一致的真正的腹部附肢原基在胚胎发育过程中消失，仅在腹侧留下三角形的退化痕迹。
而其他蠋式幼虫（粘虫和麦叶蜂）的腹足为原生构造，直接由腹足原基发育而来，其中粘虫在胚胎期与胸足原基着生位置相同，而麦叶蜂则与蝎蛉相似，其腹足的着生位置更靠近内侧的腹中线。粘虫和麦叶蜂的腹足原基最终发育形成发达的腹足，作为重要的运动器官。与之相比，长翅目蝎蛉科和蚊蝎蛉科幼虫短小的腹足基本无行动功能，很可能是为保护腹部腹面而衍生出的次生适应性构造。
由此我们认为，蝎蛉腹足并非真正的腹部附肢，腹足与胸足也并非为系列同源；而其他蠋式幼虫的腹足无论是从起源还是从功能和形态上都各不相同，因此其腹足并不具同源关系，极有可能是独立演化而来。根据腹足的不同起源，我们对蠋式幼虫的概念进行了初步修订，认为蠋式幼虫应分为原生型和次生型两种。
Mecoptera is one of the most primitive orders in holometabolous insects because theybear a pair of prominent compound eyes in the larval stage, representing the intermediate linkbetween the Holometabola and Hemimetabola and occupying an important position inphylogenetic study of insect (especially in Holometabola). Study on the organogeneticfeatures and appendage homology in Mecoptera embryogenesis can help explore thephylogenetics and evolution of the holometabolous insects based on both morphogensis andevolutionary aspects.
Based on the comparative embryology, histology and ultrastructural methods, we usedlight and electronic microscopy techniques to study the embryonic development ofPanorpidae in detail, in attempt to solve some long-standing controversial problems, such asthe homology between mandibles and maxillia, organogenesis (including embryonicmembrane, the alimentary canal, and nervous system), and the homology of thorax legs andprolegs. Combining with the abdominal appendages in representative species of othereruciform larvae Leucania separate (Lepidoptera) and Dolerus tritici (Hymenoptera), as wellas Bittacus planus (Mecoptera), we analyzed the developmental models of eruciform larvae,explored the origin and evolution of prolegs in different insect groups, and further revealedtheir homology. Our study may provide more evidences for the phylogenetic and evolutionarystudies of the holometabolous insects. The main results are as follows:
The segmentation on the mandible of Panorpidae is unconspicuous in early stage anddistinct in middle stage of the embryonic development. As the development of mandibles anddifferentiation of the molar lobe and incisor lobe, the basal segment of the mandible isgradually disappeared. Based on the segmentation, we considered that the mandible consistsof two parts, the smaller basal mandibular subcoxa and longer distal mandibular coxa. Thereduced mandibular subcoxa is homologous with the cardo of maxilla. The molar and incisorlobes are endites, serially homologous with the lacinia and galea of maxilla, respectively.
The results show that the invaginations of stomatodeum and proctodeum of Panorpobtusa are formed by the ectoderm, simultaneously occurring at the surface of embryonichead center and the end of abdominal segment. Six Malpighian tubules are derived from theectodermal processes at the end of lateral proctodaeum wall. The midgut originates from the endodermal cell bands, which are situated at the anterior and posterior embryo. Two pairedcell bands in both directions combine together and extend towards each other, finally enclosethe yolks and form the midgut rudiment. The ganglion cells formed by the neuroblast take animportant role in ganglion, nerve fiber, and lateral nerve cord formations.
During the investigation of the thoracic and abdominal appendage development ofDicerapanorpa magna, we found that the thoracic leg rudiments are located at the lateralsides in each segment and finally develop as the five-segmented thoracic legs, including coxa,femur, tibia, tarsus, and pretarsus. Compared with the thoracic legs, the proleg primordia aresituated at the inner side near the midventral line of the abdomen. The primary true abdominalappendages along the same line of the thoracic legs are disappeared gradually duringembryogenesis, only leaving flat vestiges on the lateral sides of the abdomen.
However, the prolegs in other eruciform larvae (Leucania separate and Dolerus tritici)are primary structures, which are developed from the proleg rudiment directly. The prolegprimordia of L. separate are located along the same line of the thoracic leg rudiments.However, the positions of the proleg primordia in both D. tritici and Panorpa obtusa aremuch closer to the inner midventral line of the abdomen. The proleg primordia of L. separateand D. tritici finally developed into stout prolegs as the important locomotion organs, whereasthe prolegs of Panorpidae and Bittacidae (Mecoptera) larvae are small and short,fundamentally no locomotory functions. The incompletely degenerated prolegs are very likelyto function as protecting the abdomen.
Hence we speculate that the prolegs of panorpids are not the true abdominal appendages.The abdominal prolegs and thoracic legs are not serially homologous. Compared with that ofMecoptera, the prolegs of other eruciform larvae are distinct in origin, function or morphology.Therefore, the prolegs are not homologous, but very likely evolve independently. Accordingto the distinct origin of the prolegs, we modified the concept of eruciform larvae temporarilyas that they can be subdivided into primitive and secondary types.
引文
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