Are abdominal prolegs serially homologous with the thoracic legs in panorpidae (Insecta: Mecoptera)? embryological evidence

It is a long standing question whether the abdominal prolegs of holometabolous insect larvae are serially homologous with their thoracic legs. The histology and ultrastructure of proleg embryonic development in the scorpionfly Panorpa magna were studied using light and scanning electron microscopy. During the early embryonic development, paired primary abdominal appendages appeared laterally in line with the thoracic legs. Several hours later, a pair of proleg primordia arose along the midventral line on each of the first eight abdominal segments mesial to the primary abdominal appendages, which then ceased to grow and eventually degenerated into flat vestiges. Histological observation showed that the thoracic legs were obviously connected with lateral thoracic muscle cells, whereas the abdominal prolegs resembled secondary outgrowths. No apparent contact was observed between the lumen of abdominal prolegs and the hemocoel. After dorsal closure, each thoracic segment bore a pair of well‐developed five‐jointed legs, whereas the prolegs were unjointed, fleshy structure. The remnants of the primary abdominal appendages could still be clearly seen in the mature embryo. On the basis of the histological and morphological observation of the embryonic development, we confirm that the abdominal prolegs of Panorpidae lack the characters of the primary appendages; hence they are not serially homologous with the thoracic legs. The reasons why the primary abdominal legs are reduced in scorpionflies are briefly discussed. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Embryonic development of the scorpionfly Panorpa emarginata Cheng with special reference to external morphology (Mecoptera: Panorpidae)

The Mecoptera are thought to be one of the most primitive groups in the Holometabola, but their embryology is rarely studied. By means of scanning electron microscopy, we studied the external features of the embryo of the scorpionfly Panorpa emarginata in middle and late development. The embryo remains in the superficial position until hatching. Embryonic development can be divided into 10 stages along with the first‐instar larva. The external features are described from the germ band to the first‐instar larva, with special reference to the components and segmentation of the head, the segmentation of abdomen and the formation of abdominal prolegs. Our results confirm that the head consists of an anterior‐most acron and six trunk segments: the labral, antennal, intercalary, mandibular, maxillary, and labial segments. The labrum is confirmed to derive from the paired appendages. Our observations also provide additional direct evidence that the abdominal prolegs are not serially homologous with the thoracic legs. The presence of the eleventh abdominal segment is clarified. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

The controversial origin of the abdominal appendage‐like processes in immature insects: Are they true segmental appendages or secondary outgrowths? (Arthropoda hexapoda)

In this article, I review the major characteristics of different types of appendage‐like processes that develop at the abdominal segments of many immature insects, and I discuss their controversial morphological value. The main question is whether the abdominal processes are derived from segmental appendages serially homologous to thoracic legs, or whether they are “secondary” outgrowths not homologous with true appendages. Morphological and embryological data, in particular, a comparison with the structure and development of the abdominal appendages in primitive apterygote hexapods, and data from developmental genetics, support the hypothesis of appendicular origin of many of the abdominal processes present in the juvenile stages of various pterygote orders. For example, the lateral processes, such as the tracheal gills in aquatic nymphs of exopterygote insects, are regarded as derived from lateral portions of appendage primordia, homologous with the abdominal styli of apterygotan insects; these processes correspond either to rudimentary telopodites or to coxal exites. The ventrolateral processes, such as the prolegs of different endopterygote insect larvae, appear to be derived from medial portions of the appendicular primordia; they correspond to coxal endites. These views lead to the rejection of Hinton's hypothesis (Hinton [1955] Trans R Entomol Soc Lond 106:455–545) according to which all the abdominal processes of insect larvae are secondary outgrowths not derived from true appendage anlagen. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Influence of RNAi knockdown for E-complex genes on the silkworm proleg development

Larvae of many holometabolous insects possess abdominal appendages called prolegs. Lepidoptera larvae have prolegs in the segments A3-A6. Functions of Lepidoptera hox genes on these abdominal appendages development is still a controversial issue. In this article, we report the use of double strand RNA (dsRNA)-mediated interference (RNAi) to dissect the function of some hox genes, specifically E-complex genes Ubx, abd-A, and Abd-B, in the ventral appendage development of the Lepidoptera silkworm, Bombyx mori. We found that Ubx RNAi caused leg identity in A1 segment, abd-A RNAi caused severe defect of abdominal prolegs and Abd-B RNAi allowed proleg identity in more posterior abdominal segments. These results confirm that Lepidoptera hox genes Ubx and Abd-B have evolved the repressing function to ventral appendage development, which is similar to those of Drosophila. However, Lepidoptera abd-A might have been modified distinctively during evolution, and has important roles in directing the development of prolegs.     

Phylogeny of the holometabolous insect orders: molecular evidence

Phylogenetic relationships among the holometabolous insect orders were reconstructed using 18S ribosomal DNA data drawn from a sample of 182 taxa representing all holometabolous insect orders and multiple outgroups. Parsimony analysis supports the monophyly of all holometabolous insect orders except for Coleoptera and Mecoptera. Mecoptera is paraphyletic with respect to Siphonaptera, which is nested within Mecoptera. Coleoptera is scattered as a paraphyletic assemblage across the tree topology. These data support a monophyletic Halteria (Strepsiptera + Diptera), Amphiesmenoptera (Trichoptera + Lepidoptera), Neuropterida (Neuroptera + (Megaloptera + Raphidioptera)), but Antliophora (Halteria + Mecoptera + Siphonaptera) and Mecopterida (Antliophora + Amphiesmenoptera) are paraphyletic. The limitations of using 18S ribosomal DNA as the sole phylogenetic marker for reconstructing insect ordinal relationships are discussed.     

Ultrastructure of the larval eye of the scorpionfly Panorpa dubia (mecoptera: Panorpidae) with implications for the evolutionary origin of holometabolous larvae

The evolutionary origin of holometabolous larvae is a long‐standing and controversial issue. The Mecoptera are unique in Holometabola for their larvae possessing a pair of compound eyes instead of stemmata. The ultrastructure of the larval eyes of the scorpionfly Panorpa dubia Chou and Wang, 1981 was investigated using transmission electron microscopy. Each ommatidium possesses a cornea, a tetrapartite eucone crystalline cone, eight retinula cells, two primary pigment cells, and an undetermined number of secondary pigment cells. The rhabdomeres of the eight retinula cells form a centrally‐fused, tiered rhabdom of four distal and four proximal retinula cells. The rhabdomeres of the four distal retinula cells extend distally into a funnel shape around the basal surface of the crystalline cone. Based on the similarity of the larval eyes of Panorpidae to the eyes of the hemimetabolous insects and the difference from the stemmata of the holometabolous larvae, the evolutionary origin of the holometabolous larvae is briefly discussed. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

Larval morphology of Panorpodes kuandianensis (Insecta,Mecoptera, Panorpodidae) and its evolutionary implications

Larval characters play a significant role in evolutionary and systematic studies of holometabolous insects. However, Panorpodidae, a derived family of Mecoptera, are largely unknown in their immature stages to date. Here, the first instar larva of the short-faced scorpionfly Panorpodes kuandianensis Zhong, Zhang & Hua, 2011 is described and illustrated using light and scanning electron microscopy. The larva of Panorpodes is remarkable for the absence of compound eyes on the head and the presence of seven small unpaired proleg-like processes along the midventral line on abdominal segments II–VIII. The homology of these unpaired appendage-like processes, their ecological adaptation, and the evolutionary implications of some larval characters of Panorpodidae are discussed.     

Characterization of abdominal appendages in the sawfly, Athalia rosae (Hymenoptera), by morphological and gene expression analyses

Larvae of the sawfly, Athalia rosae, have remarkable abdominal prolegs. We analyzed the morphogenesis of appendages and the expression of decapentaplegic and Distal-less genes during embryonic development to characterize the origin of prolegs. Proleg primordia in abdominal segments A1–A9 appeared shortly after the inner lobes (endites) of gnathal appendages were formed. These were located on the ventral plates, medioventral to the appendages of the other segments in light of serial homology. Nothing was seen where the main axis of the appendage should develop in abdominal segments. The primordia in A1 and A9 disappeared before larval hatching. Anal prolegs appeared separate from cerci, the main axes of appendages, which were formed temporarily in A11. The expression of decapentaplegic, which reflects the primary determination of appendages, was detected in the lateral juxtaposition with the prolegs. Distal-less was expressed in the main axes of appendages, protruding endites and the cerci, but not in prolegs and anal prolegs or the gnathal endites which do not protrude. These findings suggest a possibility that the abdominal and anal prolegs of A. rosae are outgrowths of ventral plates which derived from coxopodal elements, but not main axes of appendages.     

The role of silk threads as lifelines for caterpillars: pattern and significance of lifeline-climbing behaviour

Abstract.  1. Most lepidopteran larvae use all of their legs (thoracic legs and abdominal prolegs) when walking on solid substrates. When caterpillars involuntarily or intentionally drop from the tree canopy, they can regain their original position by climbing silk lifelines spun out from the head spinnerets. However, the taxonomic distribution of this climbing behaviour in the Lepidoptera is unknown.
2. Here, lifeline-climbing behaviour is reported in 13 lepidopteran species belonging to different taxa (five superfamilies and six families: Zygaenidae, Drepanidae, Geometridae, Lymantriidae, Noctuidae, and Nymphalidae). Caterpillars usually used only the three pairs of thoracic legs to climb lifelines, although they use different methods to walk on solid substrates, according to their taxonomic grouping and number of prolegs.
3. Results suggest that lifeline-climbing behaviour using only the thoracic legs is common among various lepidopteran taxa. The majority of species (12 of 13) climbed lifelines by alternating movement of the left and right set of thoracic legs, aided by side-to-side body movements. Only one of the 13 species, the geometrid Naxa seriaria (Motschulsky), climbed lifelines by drawing them down with its thoracic legs, aided by abdominal looping movements. While side-to-side movement of the abdomen was previously reported in lifeline climbing, this is the first report of the use of looping movements.     

Larval morphology of the scorpionfly Dicerapanorpa magna (Chou) (Mecoptera: Panorpidae) and its adaptive significance

Larval morphology can provide valuable characters for taxonomic and phylogenetic analyses of insects and reflect the adaptations to various living habits. Compared with the adult stages, larval study has lagged far behind in Mecoptera. Although several genera of Panorpidae have been studied for their larval stages, the larva of Dicerapanorpa Zhong and Hua, 2013 basically remains unclear. Here the larva of Dicerapanorpa magna (Chou) is described and illustrated in detail for the first time using light microscopy and scanning electron microscopy. The larva is eruciform, with eight pairs of abdominal prolegs in addition to three pairs of thoracic legs, as in other Panorpidae. The most remarkable characteristics of the larvae include a pair of erect subdorsal annulated processes each on abdominal segments I–IX (A1–A9) and a single middorsal annulated process on A10, as well as a pair of prominent compound eyes composed of over 40 ommatidia, which distinguish this genus from other genera of Panorpidae. The annulated processes may have adaptive significance for fossorial and soil-living habits.     

Early development of leg and wing primordia in the Drosophila embryo

The development of the leg and wing primordia in the Drosophila embryo has been traced using molecular markers. Distal-less and disconnected gene expression provide molecular labels for the leg primordia throughout embryonic development, disconnected expression in the developing leg primordia depends on Distal-less activity. The leg primordia arise as discrete clusters of cells that occupy well defined positions in the embryonic ectoderm. At later stages of embryogenesis the primordia become morphologically recognizable and are intimately associated with the development of the Keilin's organs. The presumptive leg disc and the Keilin's organ appear to derive from a common primordium. Similarly the Abnormal leg pattern gene provides a molecular label for the wing and haltere primordia. The dorsal thoracic primordia appear to be of independent origin from the legs.     

长蝎蛉幼期形态附生物学记述

【目的】蝎蛉科(Panorpidae)是长翅目(Mecoptera)最大的科,是重要的生态指示昆虫。然而,由于对环境条件要求苛刻,饲养困难,其幼期研究很不充分。【方法】本研究通过人工饲养成虫获得了长蝎蛉Panorpa macrostyla Hua的卵、幼虫和蛹等全部虫态,运用光学显微镜和扫描电子显微技术观察了其超微形态,并简要记载了其生物学特性。【结果】长蝎蛉每年发生1代,成虫发生于6月末至8月初。卵椭球形,卵壳表面覆盖一层隆起的网状结构。幼虫蠋型,具3对分4节的胸足和8对不分节的腹足;头壳高度骨化,具1对由26个小眼组成的复眼和1对3节的触角,口器咀嚼式;腹部第1-9节背面具有成对的背毛突,第10节仅有1根背毛突,腹部末端具有一个可伸缩的吸盘;呼吸系统为周气门式,具1对前胸气门和8对腹气门。幼虫共4个龄期,以预蛹期在土室内越冬。蛹为强颚离蛹,外形接近成虫,雄蛹腹部末端膨大。【结论】基于幼虫形态特征,长蝎蛉明显区别于新蝎蛉属Neopanorpa、华蝎蛉属Sinopanorpa、双角蝎蛉属Dicerapanorpa以及单角蝎蛉属Cerapanorpa幼虫。然而,长蝎蛉幼虫头部刚毛L2和SO2,腹部末节刚毛D2,SD1和SD2端部均膨大呈棒状,与蝎蛉属Panorpa其他种类区别明显,表明长蝎蛉的属级地位需要进一步研究。     

Abd-B suppresses lepidopteran proleg development in posterior abdomen

Pterygotes lack abdominal appendages except for pleuropods and prolegs. The larvae of some holometabolous insects develop prolegs, which are used for locomotion. We analyzed the role of the homeotic genes abd-A and Abd-B in lepidopteran proleg development using mutant analysis and embryonic RNAi in the silkworm Bombyx mori. The E^Mu mutant developed extra prolegs in its posterior abdomen and showed the misexpression of both genes, suggesting their involvement in proleg formation. The depletion of Abd-B by embryonic RNAi caused the development of extra prolegs on all segments posterior to A6, indicating the suppressive function of Abd-B. The abd-A RNAi animals failed to develop prolegs. These results indicate that abd-A and Abd-B are involved in proleg development in B. mori.     

Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia

The nature and origin of the arthropod labrum is a matter much under dispute. We show here that in Tribolium castaneum (Herbst, 1797) the labrum develops from two individual primordia, termed labral buds. Expression of the genes decapentaplegic (dpp) and wingless (wg) in these buds is identical to the buds of the metameric appendages (e.g. thoracic legs), except that the patterns are reversed. We propose that this reversal is the result of the rotation of the labral buds through an angle of approximately 180°. We also for the first time study dpp and wg expression in the fully developed labrum of older embryonic stages. Here, gene expression patterns show that the labrum proper is formed by fusion of the labral buds along their dorsal sides, while their ventral sides are facing outward forming the lateral sides of the fused labrum. Furthermore, we show that there are very similar patterns in another arthropod species, the spider Cupiennius salei (Keyserling, 1877), although in this species the labrum develops as a single structure and not from two separate primordia. However, in C. salei the expression of engrailed is also reversed in addition to the reversal of dpp and wg expression: engrailed is expressed in the anterior half of the labrum, and not in the posterior half like in the remaining appendages. Our results suggest that the arthropod labrum is derived evolutionarily from paired limb-bud-like primordia by rotation and fusion, and that this process is recapitulated ontogenetically to a different extent in different arthropod species.     

Embryonic development of a whirligig beetle,Dineutus mellyi,with special reference to external morphology (insecta: Coleoptera,Gyrinidae)

The egg morphology and successive changes of developing embryos of the whirligig beetle, Dineutus mellyi (Adephaga: Gyrinidae) are described from observations based on light and scanning electron microscopy. The egg surface is characterized by minute conical projections covering the entire egg surface, a stalk‐like micropylar projection at the anterior pole of the egg, and a longitudinal split line along which the chorion is cleaved during the middle embryonic stages. The germ band or embryo is formed on the ventral egg surface, and develops on the surface throughout the egg period; thus, the egg is a superficial type, as is the case in most coleopteran species. A pair of lateral tracheal gills (LTGs) of the first abdominal segment originates from appendage‐like projections arising at the lateral side of pleuropodia, and the LTGs of the second to ninth abdominal segments are arranged in a row with that of the first segment. Therefore, LTGs are structures with serial homology. The paired dorsal tracheal gills (DTGs) of the ninth abdominal segment are formed on the regions just latero‐dorsal to the LTGs of this segment. Regarding the pleuropodia as the structures being homologous with thoracic legs, neither the LTGs nor DTGs are homologous with thoracic legs, but originate in the more lateral region corresponding to the future pleura of the thoracic segments. The last (10th) abdominal segment in the larva is formed by the fusion of the embryonic 10th and 11th abdominal segments. Four terminal hooks at the end of the last abdominal segment originate from two pairs of swellings on the posterior end of the embryonic 11th abdominal segment. It is proposed that the terminal hooks possibly correspond to the claws of medially fused cerci of the embryonic 11th abdominal segment. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Cloning of a<Emphasis Type="Italic"> decapentaplegic</Emphasis> orthologue from the sawfly,<Emphasis Type="Italic"> Athalia rosae</Emphasis> (Hymenoptera), and its expression in the embryonic appendages

The cDNA of a decapentaplegic (dpp) orthologue from the sawfly, Athalia rosae (Hymenoptera), was cloned and characterized. The clone (Ar dpp) was 2,566 bp long and encoded 395 amino acids in a single open reading frame. Genomic Southern blotting showed that Ar dpp is a single copy gene. The deduced amino acid sequence can be aligned along its entire length with known insect DPPs. It shared common characteristics such as a signal sequence, a pro-domain region, and a ligand domain with seven cysteines at conserved locations. Ar dpp was expressed as a single 5.0-kb mRNA in embryos, larvae, pupae and adults. In situ hybridization showed that Ar dpp was expressed in the dorsal region proper in early embryonic stages and in the embryonic appendages of cephalic segments (labrum, antenna, mandible, maxilla, and labium), thoracic segments (thoracic legs), and all abdominal segments except the tenth segment (pleuropodia and proleg primordia). The present results indicate that Ar dpp expression reflects the primary determination of embryonic appendages.Edited by D. TautzThe sequence reported in this paper has been deposited in the DDBJ/EMBL/GenBank database with the accession number AB121072     

The effect of manipulating ecdysteroid signaling on embryonic eye development in the locust<Emphasis Type="Italic"> Schistocerca americana</Emphasis>

Adult body plan differentiation in holometabolous insects depends on global induction and control by ecdysteroid hormones during the final phase of postembryogenesis. Studies in Drosophila melanogaster and Manduca sexta have shown that this pertains also to the development of the compound eye retina. It is unclear whether the hormonal control of postembryonic eye development in holometabolous insects represents evolutionary novelty or heritage from hemimetabolous insects, which develop compound eyes during embryogenesis. We therefore investigated the effect of manipulating ecdysteroid signaling in cultured embryonic eye primordia of the American desert locust Schistocerca americana, in which ecdysteroid level changes are known to induce three rounds of embryonic molt. Although at a considerably reduced rate compared to in vivo development, early differentiation and terminal maturation of the embryonic retina was observed in culture even if challenged with the ecdysteroid antagonist cucurbitacin B. Supplementing cultures with 20-hydroxyecdysone (20E) accelerated differentiation and maturation, and enhanced cell proliferation. Considering these results, and the relation between retina differentiation and ecdysteroid level changes during locust embryogenesis, we conclude that ecdysteroids are not an essential but possibly a modulatory component of embryonic retina development in S. americana. We furthermore found evidence that 20E initiated precocious epithelial morphogenesis of the posterior retinal margin indicating a more general role of ecdysteroids in insect embryogenesis.Electronic Supplementary Material Supplementary material is available in the online version of this article at Edited by C. Desplan     

Wing-waving behaviors are used for conspecific display in the Japanese scorpionfly,Panorpa japonica

Journal of Ethology - Species of scorpionfly (Mecoptera) in the family Panorpidae perform wing-waving behaviors, whereby they rotate their front and rear wings at the same time. Previous studies...     

Histology and ultrastructure of the salivary glands and salivary pumps in the scorpionfly Panorpa obtusa (Mecoptera: Panorpidae)

Liu, S. and Hua, B. 2009. Histology and ultrastructure of the salivary glands and salivary pumps in the scorpionfly Panorpa obtusa (Mecoptera: Panorpidae). —Acta Zoologica (Stockholm) 91 : 457–465. The morphology, histology and ultrastructure of the salivary glands and salivary pumps in the scorpionfly Panorpa obtusa Cheng 1949 were investigated using light microscopy and scanning and transmission electron microscopy. The salivary glands display a distinct sexual dimorphism. The female has only two small sac‐like glands located in the prothorax, while the male possesses six long tubular glands extending into the sixth abdominal segment. The male salivary glands can be divided into five distinct regions. The apical long, thin secretory region possesses numerous secretory cells containing large secretory vesicles; the salivary reservoir expands in diameter, accumulating and temporarily storing the saliva in addition to secreting saliva; the constricted region contains prismatic cells with complex infolded plasma membrane; the sac has an internal brush border to absorb water and ions; the common salivary duct contains longitudinal muscles in the male, but not in the female. The salivary pump possesses independent strong dorsal muscles and abundant internal palm spines near its orifice. The anatomy and ultrastructure of the salivary glands and the salivary pump of scorpionflies as well as their possible functions are briefly discussed.