Anatomical changes in the neuromuscular complex of the proleg of Galleria mellonella (L.) (Lepidoptera: Pyralidiadae) during metamorphosis

The lateral and ventral external surfaces of the third and fourth abdominal segments were described and muscle attachments were correlated with surface indentations of the larva. The proleg of this species has a symmetrical planta with a complete circle of crochets. Furthermore, it differs externally from the grasping type of proleg in having a largely membranous coxal region confluent with the body wall, and a relatively large subcoxal lobe. The body wall musculature and innervation of the third and fourth abdominal segments are similar in many respects to those described for other lepidopteran larvae to which they are here compared, but differ from most because of the simpler structure of the prolegs which lack highly developed adductor muscles. Like most muscles innervated by the ventral nerve, the principal plantar retractors of these two segments cease to function in the first day of the pupal stage and have completely degenerated by the forty-fifth hour of pupal life. The ventral nerve retains its four primary branches in the adult, in which many smaller rami can be traced to the cuticle and to the neoblastic body wall muscles.     

Three-dimensional reconstruction of the musculature of Cossura pygodactylata Jones, 1956 (Annelida: Cossuridae)

The musculature of adult specimens of Cossura pygodactylata was studied by means of F-actin labelling and confocal laser scanning microscopy (CLSM). Their body wall is comprised of five longitudinal muscle bands: two dorsal, two ventral and one ventromedial. Complete circular fibres are found only in the abdominal region, and they are developed only on the border of the segments. Thoracic and posterior body regions contain only transverse fibres ending near the ventral longitudinal bands. Almost-complete rings of transverse muscles, with gaps on the dorsal and ventral sides, surround the terminal part of the pygidium. Four longitudinal bands go to the middle of the prostomium and 5–14 paired dorso-ventral muscle fibres arise in its distal part. Each buccal tentacle contains one thick and two thin longitudinal muscle filaments; thick muscle fibres from all tentacles merge, forming left and right tentacle protractors rooted in the dorsal longitudinal bands of the body wall. The circumbuccal complex includes well-developed upper and lower lips. These lips contain an outer layer of transverse fibres, and the lower lip also contains inner oblique muscles going to the dorsal longitudinal bands. The branchial filament contains two longitudinal muscle fibres that do not connect with the body musculature. The parapodial complex includes strong intersegmental and segmental oblique muscles in the thoracic region only; chaetal retractors, protractors and muscles of the body wall are present in all body regions. Muscle fibres are developed in the dorsal and ventral mesenteries. One semi-circular fibre is developed on the border of each segment and is most likely embedded in the dissepiment. The intestine has thin circular fibres along its full length. The dorsal blood vessel has strong muscle fibres that cover its anterior part, which is called the heart. It consists of short longitudinal elements forming regular rings and inner partitions. The musculature of C. pygodactylata includes some elements that are homologous with similar muscular components in other polychaetes (i.e., the body wall and most parapodial muscles) and several unique features, mostly at the anterior end.     

The Musculature of <Emphasis Type="Italic">Testudinella patina</Emphasis> (Rotifera: Flosculariacea), Revealed with CLSM

The musculature of Testudinella patina was visualized using phalloidin-linked fluorescent dye by confocal laser scanning microscopy. The conspicuous broad retractors appear to be made up of five separate fibers, of which three anchor in the neck region whereas two extend into the corona. Besides the broad retractors, a total of five paired longitudinal retractors are present and all of them extend into the corona. Incomplete circular muscles are found in groups in the neck region and in the medial and posterior parts of the trunk. The foot musculature comprises eight thin ventral foot muscles and six thicker dorsal foot muscles that all extend from the foot basis to the distal part of the foot. At the basis of the foot, each of the dorsal foot muscles anchors on a smaller, S-shaped subterminal foot muscle. The foot musculature furthermore comprises one pair of paraterminal foot muscles that each anchors basally on a subterminal foot muscle, extends into the most proximal part of the foot and attaches on one of the dorsal foot muscles. The visceral musculature is composed of extremely delicate fibers and is restricted to an area around and posterior to the foot opening. The presence of incomplete circular muscles supports that these muscles are a basal trait for Rotifera, whereas the morphology of the broad retractors and foot muscles is much more specialized and may be autapomorphic for Testudinella or alternatively for this genus and its closest relatives. The present results stress that revealing muscles by staining may produce new information from even well-investigated species, and that this information may contribute to a better understanding of functional as well as phylogenetic aspects of rotifer biology.     

Functional morphology of the muscles in Philodina sp. (Rotifera: Bdelloidea)

Whole-mounts of Philodina sp., a bdelloid rotifer, were stained with fluorescent-labeled phalloidin to visualize the musculature. Several different muscle types were identified including incomplete circular bands, coronal retractors and foot retractors. Based on the position of the larger muscle bands in the body wall, their function during creeping locomotion and tun formation was inferred. Bdelloid creeping begins with the contraction of incomplete circular muscle bands against the hydrostatic pseudocoel, resulting in an anterior elongation of the body. One or more sets of ventral longitudinal muscles then contract bringing the rostrum into contact with the substrate, where it presumably attaches via adhesive glands. Different sets of ventral longitudinal muscles, foot and trunk retractors, function to pull the body forward. These same longitudinal muscle sets are also used in `tun' formation, in which the head and foot are withdrawn into the body. Three sets of longitudinal muscles supply the head region (anterior head segments) and function in withdrawal of the corona and rostrum. Two additional pairs of longitudinal muscles function to retract the anterior trunk segments immediately behind the head, and approximately five sets of longitudinal retractors are involved in the withdrawal of the foot and posterior toes. To achieve a greater understanding of rotifer behavior, it is important to elucidate the structural complexity of body wall muscles in rotifers. The utility of fluorescently-labeled phalloidin for the visualization of these muscles is discussed and placed in the context of rotifer functional morphology.     

Rotifer muscles as revealed by phalloidin-TRITC staining and confocal scanning laser microscopy

By combining phalloidin‐TRITC staining with confocal scanning laser microscopy (CSLM), the pattern of the musculature in two species of Rotifera, Euchlanis dilatata unisetata and Brachionus quadridentatus is revealed. The same general muscle pattern prevails in both species. The major components of the body wall musculature are: 1. retractor muscles (5 pairs in E. dilatata unisetata and 3 pairs in B. quadridentatus); 2. Two pairs of dorso‐ventral muscles; 3. Two pairs of perpendicular muscles (in E. dilatata unisetata); 4. retractors of the corona (median, lateral and ventral); 5. Foot retractors. In addition, three pairs of cutaneo‐visceral muscles and visceral muscles (including mastax muscles) are described. The sphincter of the corona was found only in B. quadridentatus. The high degree of muscle differentiation points to a high level of development of rotifer muscular system.     

Musculature in three species of <Emphasis Type="Italic">Proales</Emphasis> (Monogononta,Rotifera) stained with phalloidin-labeled fluorescent dye

The musculature in the rotifer species Proales daphnicola, P. reinhardti and P. fallaciosa was stained with phalloidin-labeled fluorescent dye and compared using confocal laser scanning microscopy. All three species share several homologous muscle systems, but each systems detailed morphology varies among the species both concerning appearance, number and location. The obtained results were compared with data from other rotifers and it was concluded that the muscles pars coronalis and the corona sphincter probably represent conditions in Ploima or Monogononta, while incomplete circular muscles and dorsal and ventral trunk retractors might be part of the eurotatorian ground pattern.     

Muscular architecture of <Emphasis Type="Italic">Milnesium tardigradum </Emphasis>and <Emphasis Type="Italic">Hypsibius </Emphasis>sp. (Eutardigrada,Tardigrada) with some data on <Emphasis Type="Italic">Ramazottius oberhaeuseri</Emphasis>

The architecture of the musculature of the eutardigrade species Milnesium tardigradum Doyère, 1840, Hypsibius sp. and Ramazzottius oberhaeuseri (Doyère in Ann Sci Nat Zool Sér 2(14):269–369, 1840) is investigated by phalloidin staining and confocal laser scanning microscopy. There are methodological problems in staining eutardigrades due to physiological alterations under stress (anhydrobiosis) and due to penetration problems of the cuticle. It is helpful to fix specimens in the state of asphyxy, where animals are stretched following an oxygen shortage in their environment. The musculatures of all three species correspond in their general architecture, but differ in detail, such as in the number of muscles. All muscles are isolated muscle strands. There are on each body side two dorsal and one ventral muscle strands, in addition to a system of dorsoventral, lateral and lateroventral muscles. Seven median ventral attachment points give rise to dorsoventral, ventrolateral and appendage muscles. The appendages receive several muscles originating dorsally and ventrally. The number of muscles and the arrangement differ in each appendage. The fourth appendage shows the greatest differences with a far smaller number of muscles compared to other species. The musculature shows comparably few strict segmental patterns, for example, the musculature of each appendage differs from the other ones. By comparison with literature data on the same species and data of Macrobiotus hufelandi it can be shown that eutardigrades have a roughly comparable muscular architecture, but that there are several differences in detail. Dedicated to Professor Westheide on the occasion of his 70th birthday.     

Anatomy and innervation of the abdominal segmental muscles in larval and adult Tenebrio molitor (Coleoptera)

The external morphology, musculature, and the innervation of the abdominal segments were examined in larvae and adult Tenebrio molitor. In the larva, there are 26 pairs of muscles arranged at four different levels in the ventral, lateral, and dorsal region of each segment. In the adult, the number of muscles has been dramatically reduced and is limited to six pairs of muscles located at the dorsal and lateral region of the segment. These muscles, in either larval or adult stages, are innervated by two main nerves, n1 and n2, which originate from the segmental ganglia. The cell bodies of the motoneurons innervating the muscles of the 3rd abdominal segment are located in the 3rd and 2nd abdominal ganglia. Some cell bodies are retained throughout metamorphosis, but others disappear during the larva-pupa transition.     

The locust abdominal muscle receptor organ: response characteristics and its role in the control of segmental distance

A single mutipolar receptor cell is located at the dorsal edge of the lateral internal dorsal muscle in each abdominal segment of the locust (Locusta migratoria). Muscle and receptor cell form the abdominal muscle receptor organ. The receptor cell monitors length changes in the intersegmental muscle, and as a consequence also detects the length of an abdominal segment (cuticule and intersegmental membrane).The muscle receptor organ responds in a phasictonic fashion. The phasic component encodes the rate of change in the stimulus independent from the prevailing length of the muscle receptor organ. The tonic component monitors the absolute length of the muscle.Stimulation of a single muscle receptor organ leads to reflex effects on the ipsilateral longitudinal muscles in at least three adjacent segments. Muscles that shorten the abdomen are activated while their extending antagonists receive reduced activity.The reflex activation of the muscles is polysynaptic. Monosynaptic connections between the receptor and the motoneurones were not found.We identified an interneurone that receives monosynaptic input from the muscle receptor organs in at least three adjacent segments. The interneurone excites motorneurones to the longitudinal muscles of the next posterior segment.Abbreviations aMROII abdominal muscle receptor interneurone 1 - AS3 third abdominal segment - AS4 fourth abdominal segment - AS5 fifth abdominal segment - AS6 sixth abdominal segment - EPSP excitatory postsynaptic potential - MN median nerve - MR multipolar receptor cell - MRO muscle receptor organ - N1 tergal nerve - N2 sternal nerve     

Musculature of an illoricate predatory rotifer Asplanchnopus multiceps as revealed by phalloidin fluorescence and confocal microscopy

The pattern of muscles in the actively swimming predatory rotifer Asplanchnopus multiceps is revealed by staining with tetramethyl-rhodamine isothiocyanate (TRITC)-labelled phalloidin and confocal scanning laser microscopy (CSLM). The major components of the musculature are: prominent semicircular muscles of the corona; paired lateral, dorsal and ventral retractors in the trunk; a network of six seemingly complete circular muscles and anastomosing longitudinal muscles in the trunk; two short foot retractors, originating from a transverse muscle in the lower third of the trunk. The sphincter of the corona marks the boundary between the head and the trunk. The muscular patterns in rotifers with different lifestyles differ clearly, therefore, the muscular patterns seem to be determined by the mode of locomotion and feeding behaviour.     

Early leaf miners and the ground plan of the lepidopteran larval trunk: Caterpillar morphology of the basal moths Heterobathmia,Eriocrania, and Acanthopteroctetes

The larval trunk morphology including chaetotaxy, locomotory structures, and trunk musculature of Heterobathmia pseuderiocrania, Eriocrania cicatricella, and Acanthopteroctetes unifascia is described using conventional light, polarization, and scanning electron microscopy. The ground plan morphology of the lepidopteran larva and neolepidopteran caterpillar is discussed in light of the life history succession from free soil dwelling organism to endophagous and finally to a primarily free living, angiosperm associated organism. I suggest that the larval morphology is argued to be strongly influenced by the shift in number of surfaces present in the larval environment. Especially the environment of the endophagous species, where the upper surface of the leaf mine is linked to the presence of dorsal locomotory structures such as the retractable calli and dorsal friction patches is proposed to have had a significant impact on the morphology and locomotory mechnism of the lepidopteran caterpillar. The chaetotaxy of the lepidopteran ground plan is found to be simple, consisting only of primary and secondary tactile setae and segmental proprioceptors. The presumption of Gerasimov ([1935] Zool Anz 112:177–194) that MXD1 of the prothorax is a shifted mesothoracic MD setae is supported. I suggest that the serial arrangement of the proprioceptors MD1, present on all trunk segments except the prothorax, and a trisetous MV group on all the thoracic segments is part of the lepidopteran larval ground plan. The absence of apodeme structures associated with trunk musculature in the nonglossatans suggests that this is an autapomorphic character of the Lepidoptera and it is further found to have been influential in the evolution of the typical caterpillar trunk. The attachments of the thoracic muscles directly to the trunk integument, suggest that the apodemal structures ancestral to the Amphiesmenoptera have been reduced in the Lepidoptera. Within the non‐Neolepidoptera, the lifehistory shift may have resulted in reduction of the dorsal locomotory structures, such as calli. The abdominal musculature and structural similarities further suggest that the ventral calli are structural predecessors to the crotchet bearing proleg of the “typical caterpillar.” J. Morphol. 274:1239–1262, 2013. © 2013 Wiley Periodicals, Inc.     

Homonomies within the ventral muscle system and the associated motoneurons in the locust,Schistocerca gregaria (Insecta,Caelifera)

To understand the segmental reiteration of an insect, the serially arranged neuromuscular system of the locust, Schistocerca gregaria, is studied. The ventral muscle system is chosen and its motoneuronal supply is described in the thoracic and pregenital segments. In general, repetitively arranged, similar sets of motoneurons (MNs) supply the ventral muscles of these segments. Common criteria of both topology of muscles and neural features (nerve branches and motoneuronal supply) suggest possible homonomies of the ventral longitudinal muscles and ventral diaphragm of the thoracic and abdominal system. Based on a segment-by-segment analysis, muscle topology and motor supply match, in most instances. There are, however, cases where such a parallelism is missing. In a particular cases the supply of apparently homonomous muscles shifts from one set of MNs to another. In another case, putatively equivalent MNs of different ganglia supply morphologically different muscle structures in the adult animal. Therefore, it becomes apparent that muscles and their supplying MNs are, in principle, independent elements which might be subjected autonomously to ontogenetic processes. As a consequence, in the search for the basic segmental Bauplan depending on homonomous structures, muscles and MNs have to be regarded as separate entities.Abbreviations A1–6 abdominal ganglion (or neuromere A1–3) - AS1–6 abdominal segment 1–6 - DUM doisal unpaired median - M muscle (number) - MN motoneuron - N nerve (number) - PMN paramedian nerve - T1–3 pro-, meso-, metathoracic ganglion - TS1–3 pro-, meso-, metathoracic segment - VD ventral diaphragm - VM ventral muscle     

Comparative analysis of the intrinsic leg musculature of the American cockroach,Periplaneta americana (L.)

The American cockroach has a total of 368 muscles inserting on the post-coxal segments of its legs. By using a narrow morphological definition for delimiting individual muscles, it is shown (i) that the protrochanteral musculatures (23 muscles/leg) differ from the essentially identical meso- and metatrochanteral musculatures (24 and 26 muscles/leg) in number and disposition of extensors and in having a completely different flexor composition, and (ii) that the musculatures of the more distal segments of the legs are completely serially homologous, there being 2 muscles for moving each femur, 23 for each tibia, 7 for each first tarsomere, and 5 for each of the paired pretarsal claws. In all six legs, the trochanteral and tibial musculatures each contain single slender muscles that may be acting proprioceptively to measure the angular displacements between, respectively, the coxas and trochanters, and the femurs and tibias. Neurological and phylogenetic considerations are used to demonstrate why a narrow morphological definition should be employed, and why the widely used functional definition of Snodgrass ('35) is not only fallacious on evolutionary grounds, but also leads to making erroneous conclusions regarding the manner in which insect musculature is controlled by the insect central nervous system. Finally, it is hypothesized that the physiological limitations imposed by having an open circulatory system and the problems inherent in the neural control of large muscles may have been major evolutionary factors in forcing insects to use many slender muscles to control their body movements.     

Musculature of Notholca acuminata (Rotifera: Ploima: Brachionidae) revealed by confocal scanning laser microscopy

Abstract. The body-wall and visceral musculature of Notholca acuminata was visualized using phalloidin-linked fluorescent dye under confocal laser scanning microscopy. The body-wall musculature includes dorsal, lateral, and ventral pairs of longitudinally oriented body retractor muscles, two pairs of head retractors, three pairs of incomplete circular muscles, which are modified into dorso-ventral muscles, and a single pair of dorsolateral muscles. The visceral musculature consists of a complex of thick muscles associated with the mastax, as well as several sets of delicate fibers associated with the corona, stomach, gut, and cloaca, including thin longitudinal gut fibers and viscero-cloacal fibers, never before reported in other species of rotifers. The dorsal, lateral, and ventral retractor muscles and the incomplete circular muscles associated with the body wall appear to be apomorphies for the Rotifera. Muscle-revealing staining shows promise for providing additional information on previously unrecognized complexity in rotifer musculature that will be useful in functional morphology and phylogenetic analyses.     

CLSM analysis of the phalloidin-stained muscle system in Nerilla antennata, Nerillidium sp. and Trochonerilla mobilis (Polychaeta; Nerillidae)

The entire muscle system of Nerilla antennata, Nerillidium sp. and Trochonerilla mobilis was three-dimensionally reconstructed from whole mounts. In juvenile and adult specimens the F-actin musculature subset was stained with FITC-conjugated phalloidin and visualized with a confocal laser scanning microscope (cLSM). The muscle system shows the following major organization: 1) circular muscles are totally absent in the body wall; 2) the longitudinal muscles are confined in two ventral and two dorsal thick bundles; 3) additional longitudinal muscles are located in the ventro- and dorsomedian axis; 4) three segmental pairs of ventral oblique muscles elongate into the periphery: the main dorsoventral muscles that run along the body side posterior and dorsally and the anterior and posterior oblique parapodial muscles, which contribute to the ventral chaetal sacs; 5) one segmental pair of dorsal oblique parapodial muscles, contributing to the dorsal chaetal sacs; 6) five to seven small dorsoventral muscles per segment; and 7) complex head and pharyngeal musculature. These results support the belief that absence of circular muscles in the polychaete body wall is much more widely distributed than is currently presumed.     

Developmental dynamics of myogenesis in the shipworm <Emphasis Type="Italic">Lyrodus pedicellatus</Emphasis> (Mollusca: Bivalvia)

Background

The shipworm Lyrodus pedicellatus is a wood-boring bivalve with an unusual vermiform body. Although its larvae are brooded, they retain the general appearance of a typical bivalve veliger-type larva. Here, we describe myogenesis of L. pedicellatus revealed by filamentous actin labelling and discuss the data in a comparative framework in order to test for homologous structures that might be part of the bivalve (larval) muscular ground pattern.

Results

Five major muscle systems were identified: a velum retractor, foot retractor, larval retractor, a distinct mantle musculature and an adductor system. For a short period of larval life, an additional ventral larval retractor is present. Early in development, a velum muscle ring and an oral velum musculature emerge. In late stages the lateral and dorsal mantle musculature, paired finger-shaped muscles, an accessory adductor and a pedal plexus are formed. Similar to other bivalve larvae, L. pedicellatus exhibits three velum retractor muscles, but in contrast to other species, one of them disappears in early stages of L. pedicellatus. The remaining two velum retractors are considerably remodelled during late larval development and are most likely incorporated into the elaborate mantle musculature of the adult.

Conclusions

To our knowledge, this is the first account of any larval retractor system that might contribute to the adult bodyplan of a (conchiferan) mollusk. A comparative analysis shows that a pedal plexus, adductors, a larval velum ring, velum retractors and a ventral larval retractor are commonly found among bivalve larvae, and thus most likely belong to the ground pattern of the bivalve larval musculature.

     

Study of architectonics of rotifer musculature by the method of fluorescence with use of confocal microscopy

Musculature of two species of rotifers Testudinella patina (Testudinellidae) and Platyias patulus (Brachiomidae) was studied in confocal laser scanning microscope (CLSM) using fluorescent-labeled phalloidin. It includes cutaneous, visceral, and cutaneus-visceral musculature. The common pattern of structure of the cutaneous musculature is represented by postcoronal circular or transverse muscles and connected with them 2–3 pairs of retractors of the trunk, dorsolateral muscles (17-4), two pairs or bundles of lateral retractors of the corona, circular muscles of the foot, and 10-2 retractors of the foot. Visceral musculature includes muscles of the mastax of both kinds. Spiral-like muscle of cloaca of the T. patina and associated with it V-shaped one as well as strong dorsolateral retractors consisting of 6 longitudinal muscle bundles are typical of Testudinellidae only. Three pairs of cutaneus-visceral muscles bind the musculature of mastax with the body surface in T. patina. Differences in localization and thickness of some elements of musculature of these species are determined by morphological peculiarities of structure of the corona, mastax, and foot, as well as by the rotifer body shape.     

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.     

Onychophoran‐like myoanatomy of the Cambrian gilled lobopodian Pambdelurion whittingtoni

Arthropods are characterized by a rigid, articulating, exoskeleton operated by a lever‐like system of segmentally arranged, antagonistic muscles. This skeletomuscular system evolved from an unsegmented body wall musculature acting on a hydrostatic skeleton, similar to that of the arthropods’ close relatives, the soft‐bodied onychophorans. Unfortunately, fossil evidence documenting this transition is scarce. Exceptionally‐preserved panarthropods from the Cambrian Lagerstätte of Sirius Passet, Greenland, including the soft‐bodied stem‐arthropod Pambdelurion whittingtoni and the hard‐bodied arthropods Kiisortoqia soperi and Campanamuta mantonae, are unique in preserving extensive musculature. Here we show that Pambdelurion's myoanatomy conforms closely to that of extant onychophorans, with unsegmented dorsal, ventral and longitudinal muscle groups in the trunk, and extrinsic and intrinsic muscles controlling the legs. Pambdelurion also possesses oblique musculature, which has previously been interpreted as an arthropodan characteristic. However, this oblique musculature appears to be confined to the cephalic region and first few body segments, and does not represent a shift towards arthropodan myoanatomy. The Sirius Passet arthropods, Kiisortoqia and Campanamuta, also possess large longitudinal muscles in the trunk, although, unlike Pambdelurion, they are segmentally divided at the tergal boundaries. Thus, the transition towards an arthropodan myoanatomy from a lobopodian ancestor probably involved the division of the peripheral longitudinal muscle into segmented units.