Resolving insect phylogeny: The significance of cephalic structures of the Nannomecoptera in understanding endopterygote relationships

The Nannomecoptera are among the most enigmatic and controversial taxa of endopterygote insects, the phylogenetic resolution of which is crucial to understanding the evolution of neopteran insects. Once considered a subordinate lineage within the Mecoptera, renewed interest in nannochoristids has been prompted by evidence that the Nannomecoptera are not admissible to the clade of extant scorpion flies but are more likely to belong to the clade Siphonaptera + Nannomecoptera + Diptera. The overarching purpose of the present account is to provide novel and extensive morphological character traits in addition to those already existing for adult structures. The aim is to determine if these traits support molecular data sets that have been suggested elsewhere to clarify the phyletic position of Nannochoristidae. This account focuses on nannomecopteran larvae, which unlike those of other mecopterans have received little attention. Thus, the thrust of this investigation is to provide detailed anatomical data on nannochoristid larvae for a targeted inquiry into their phylogenetic affinities. The described characters are discussed and presented in a data matrix comprising representatives of all endopterygote orders. While the study is based primarily on the New Zealand species Nannochorista philpotti, it is proposed that all nannomecopteran larvae will prove to be similar to this taxon in most if not all structural features of significance to a higher-level phylogenetic context.     

Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications

External and internal head structures of Caurinus dectes were examined and described in detail. The features are compared to conditions found in other groups of Antliophora. Caurinus is obviously crucial for the reconstruction of the mecopteran and antliophoran groundplan. It displays a remarkable series of plesiomorphic character states such as a complete clypeolabral suture, the presence of M. hypopharyngomandibularis (M. 13) and M. frontohypopharyngalis (M. 41), a subdivided clypeus, a short head without rostrum, a dorsal tentorial arm attached to the head capsule, the absence of a cranial dilator of the antenna, and large mandibles with a well developed apical tooth, two distinct subapical teeth, and a basal molar part. The first three plesiomorphic features render potential autapomorphies of Mecoptera in the traditional sense invalid. Autapomorphies of Caurinus are the distinctly flattened labrum, the absence of the labroepipharyngeal muscle, the very large size of M. 13, the strongly enlarged penultimate palpomeres, the partition of M. 41, the very strongly developed precerebral sucking chamber, strongly curved optic lobes, the presence of a large protocerebral extension in the genal region and deep posterior excavations of the protocerebrum. The maxillolabial plate, the absence of cardines as separate structures, the reduction of ocelli, and the origin of maxillary palp muscles on a median ridge or area of the maxillolabial plate are likely autapomorphies of Boreidae. Another potential autapomorphy of the family is the presence of longitudinal furrows on the mandibles. However, they are absent in Boreus. The thick strongly sclerotised, median ridge of the maxillolabial plate, the missing retractibility of the prementum, the absence of extrinsic labial muscles, and the presence of a median ridge on the prepharyngeal roof suggest a clade Boreus + Hesperoboreus. The origin of extrinsic maxillary muscles from the clypeus has probably evolved independently in Boreus and Hesperoboreus, and in Panorpa, respectively. The absence of M. craniolacinialis and the presence of a row of several subapical mandibular teeth are autapomorphies of Boreus. The presence of a specific intrinsic muscle of the salivary duct and a membranous galea enclosing the labrum and mandibular base are derived features shared by Boreidae and Pistillifera (galea absent in Nannochorista, Siphonaptera and Diptera). The loss of M. frontolabralis (M. 8) is a potential apomorphy of Mecoptera incl. Siphonaptera. A sister group relationship between Boreidae and Siphonaptera is not supported by characters of the adult head. Head structures of Siphonaptera are extremely modified in correlation with ectoparasitic habits.     

Comparative morphological assessment and phylogenetic significance of the wing base articulation in Psylloidea (Insecta,Hemiptera, Sternorrhyncha)

The wing articulation sclerites, as well as wing base environment, of phylogenetically distant Psylloidea taxa were examined by optical and electron microscopy in order to estimate the phylogenetic significance of observed morphological patterns. The basiradial bridge is strongly developed and links the fused humeral plate, basisubcostale, basiradiale and second axillary sclerite to the fused veins R + M + Cu. The proximal median plate has a vertical orientation, which may have a role in moving the wing forward and backward. The weak sclerotization posteriad of the second axillary sclerite and anteriad to the third axillary sclerite facilitates the backward movement of the wing. The horizontal hinge (= basal hinge), the vertical hinge and the torsional hinge are the most important fold- and flexion-lines for the mobility of the wing, whereas humeral folds and the anterior axillary fold-line play a minor role. The basalare presents two horns or processes that are autapomorphic traits for the superfamily Psylloidea. The monophyly of Psylloidea is also supported by the absence of the subalare, of the median notal wing process and of the anterior arm of the third axillary sclerite (lacking articulation with second axillary sclerite). Major interspecific variations are observed in tegula, first axillary sclerite and basalare shape and size. The second distal median plate is absent in Homotoma ficus (Homotomidae) and Glycaspis brimblecombei (Spondyliaspidinae), whereas it is present in Calophya schini (Calophyidae) and Psylla buxi (Psyllinae/Arytaininae); the presence of this sclerite could be a synapomorphy linking Calophyidae and the “psyllid assemblage”.     

The gonangulum: A reassessment of its morphology,homology, and phylogenetic significance

The gonangulum is a sclerite in the female genitalic region of insects. Its presence or full development has long been considered an apomorphy supporting Zygentoma + Pterygota. Recent studies of female genitalia in several insect orders (K.-D. Klass and co-workers) revealed many new data on the gonangulum and homologous sclerotisations (laterocoxa LC9). Herein the gonangulum area is described (including articulations, muscle attachments, sulci) and compared among Archaeognatha, Zygentoma, Odonata, Dermaptera, Dictyoptera, and Notoptera. A wider perspective is provided to the topic by addressing some novel issues: identification of LC9 sclerotisations in non-insect taxa and in insects that secondarily lack an ovipositor; occurrence of homonomous sclerotisations in other abdominal segments of both sexes; morphological interpretation of LC9; and the role of paedomorphosis in LC9 evolution. As a result, there is currently no support for any insect lineage from this character system. For gonangulum-related characters both a significant intra-ordinal variation and frequent homoplasy are demonstrated using various Odonata, Dermaptera, and Dictyoptera as examples. Divergent fates of LC9 in simplified genitalia are shown using a dermapteran and an odonatan. We view all this as a showcase of how a renewed and more detailed examination of a character system can dramatically change the phylogenetic evidence drawn from it.     

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.     

Comparative morphology and evolutionary aspects of the reflective under wing scale-pattern in Fritillary butterflies (Nymphalidae: Argynnini)

The wing scale ultrastructure of the reflective under wing pattern found in many Argynnini butterflies are examined for all recognised genera and subgenera and compared to that of some basal Heliconiini. A true reflective pattern probably evolved once within the Argynnini. But the phylogenetic information in these structures is limited due to a high degree of homoplasy in the scale ultrastructure related to the reflective patterns. The degree of specialisation is also homoplastic. The general morphological modification responsible for the reflective patterns seems to be a “closing” of the large windows, which generally occupy most of the inter-ridge space on the abwing surface in the scales of higher Lepidoptera. The fact that the Argynnis niobe morphs with a silvery pattern have scales with ‘closed windows’ whereas the Argynnis niobe morphs without a silvery pattern have typical non-reflective scales with very large windows supports this conclusion.The degrees of modification of the scales, including whether both cover and ground scales or only cover scales are modified, are to some extent correlated to the degree of reflectiveness in the wing pattern. Boloria eunomia has, as the only species, more modified ground scales than cover scales.     

Apotrachelocerca arenicola (Kahl, 1933) n. g., comb. n. (Protozoa, Ciliophora, Trachelocercidae): morphology and phylogeny

During faunistic study on psammophilic ciliates along the coast of Qingdao, China, a population of Trachelocerca arenicola Kahl, 1933 was found and then investigated using silver staining and gene sequencing methods. The results indicated that it represented a new genus Apotrachelocerca characterized by uninterrupted circumoral kineties composed of two rows of dikinetids and no brosse or ciliary tuft in the oral cavity. This new genus should be assigned to the family Prototrachelocercidae Foissner, 1996. Based on the small subunit rRNA gene sequence, phylogenetic trees revealed that Apotrachelocerca arenicola occupied a basal position to other trachelocercids.     

The preoral cavity of lower Hymenoptera (Insecta): comparative morphology and phylogenetic significance

The skeletal and muscular morphology of the preoral cavity, including the labrum, hypopharynx and labium, was examined in the imago in representatives of all the ‘symphytan’ families as well as the apocritan families Stephanidae, Megalyridae and Trigonalyidae. Xyelidae have complex modifications for masticating pollen, remarkably similiar to those of primitive Lepidoptera. These modifications, collectively termed the triturating basket complex, include an asymmetrical distal epipharyngeal wall with a microtrichial brush and an enlarged infrabuccal pouch with heavy cuticular armature that interacts with the mandibles during feeding. There were striking structural differences between the two subfamilies of Xyelidae in the ligular region; the reduced glossa and clubshaped paraglossae of Macroxyelinae resembles those of primitive Lepidoptera, while the well developed, flattened glossa and paraglossae in Xyelidae are similiar to those of most other ‘Symphyta’. A putative transformation series, leading from a relatively large labrum with unsclerotised distal epipharyngeal wall lying anterior to the mandibles, as seen in Xyelidae and enthredinoidea, to a small and heavily sclerotised labrum and distal epipharyngeal wall lying posterior to the mandibles, as seen in ‘Siricoidea’, Orussidae and the Apocrita, was revealed. These modifications may be adaptations to enable the adult of the families pupating in wood to emerge from the pupal chamber. The Anaxyelidae, Orussidae and Apocrita have similiar configurations of the glossa and nsertions of the ventral premental adductors. This indicates a close affinity of the Anaxyelidae to Orussidae + Apocrita, a hypothesis that is in conflict with other character systems. The Orussidae and Stephanidae share a unique condition in the development of a pair of large apodemes attached to the labrum; this renders the groundplan state of the labrum in the Apocrita uncertain. Twentyfive characters were defined in an attempt to eludicate the ‘Symphyta’–Apocrita transition. A numerical cladistic analysis of the characters was undertaken, resulting in 522 minimum length trees. The characters are also discussed with reference to a cladogram which resulted from an analysis of the characters derived from the present study and a survey of characters from literature.     

The flagellin gene of Borrelia miyamotoi sp. nov. and its phylogenetic relationship among Borrelia species

Abstract We have cloned and sequenced the flagellin gene from Borrelia miyamotoi strain HT31 and compared it with previously published flagellin sequences. Sequence similarity analysis demonstrated that strain HT31 is phylogenetically distant from the three species of Lyme disease borreliae and is deeply branched into the relapsing fever borrelia cluster. The result was in full agreement with the classification of Borrelia strains using 16S rRNA sequences. This finding indicates that a phylogenetic analysis using flagellin gene sequences might be useful for classification of Borrelia strains.     

On the morphology of spermatozoa in some African murines (Rodentia, Muridae): the taxonomic and phylogenetic aspects

A comparative analysis of sperm-head morphology and measurements in 17 species from nine genera of African Murinae: Rattus rattus, Mastomys coucha, M. huberti, M. erythroleucus, Mastomys sp. 2, Praomys albipes, P. fumatus, Mus mahomet, Arvicanthis somalicus, A. abyssinicus, A. dembeensis, Arvicanthis sp., Lemniscomys macculus, Pelomys harringtoni, Acomys cahirinus, Acomys sp., Uranomys ruddi, was carried out. Spermatozoa of all examined species are of the same basic type. They consist of an asymmetrical head, falciform or scythelike in shape, and a tail attached to the ventrocaudal surface of the head. There are great interspecific differences in sperm morphology and size. The significance of this variation for estimation of taxonomic aspects and phylogenetic relationships among the species, as well as between them and other groups, is discussed. The sperm morphology supports a close evolutionary relationship among the genera Lemniscomys and Arvicanthis. It also indicates that Pelomys is distinctive. The relationships between Acomys and Uranomys are discussed.     

The sperm ultrastructure of Caurinus dectes Russell (Mecoptera: Boreidae) and its phylogenetic implications

The sperm structure of the enigmatic mecopteran species Caurinus dectes (Boreidae) is described for the first time. Diagnostic features are the bi-layered acrosome, a cylindric nucleus provided with two longitudinal opposite grooves, and a simple 9 + 2 axoneme which degenerates in the posterior tail end. The results are conform with the monophyly of Mecoptera including Boreidae. A possible autapomorphy of the order is the presence of the two longitudinal opposite grooves along the nucleus, and the presence of two electron-dense fibres beneath the axoneme. Some apparently plesiomorphic features are preserved in the sperm of Caurinus. Features characterizing the distal part of the flagellum, including the presence of an axial cylindrical structure and the distinctive type of axoneme degeneration, are potential synapomorphies of Caurinus and Boreus, i.e. autapomorphic traits of Boreidae.     

Cleavage in<Emphasis Type="Italic"> Nemertoderma westbladi</Emphasis> (Nemertodermatida) and its phylogenetic significance

Recent phylogenetic analyses of ribosomal and protein coding nuclear genes place the marine worms within the Nemertodermatida as one of the oldest lineages among the bilaterian animals. We studied the early embryonic cleavage in Nemertoderma westbladi to provide the first account of nemertodermatid early development. Live embryos were studied with interference microscopy and fixed embryos were either sectioned or studied with confocal laser scanning microscopy. Initially the divisions in the embryo are radial, but then micromeres are shifted clockwise generating a spiral pattern. The four-cell stage is characterized by duets of macromeres and micromeres and thus resembles the duet cleavage reported from members of the Acoela. However, subsequent stages differ from the acoel duet pattern and also from quartet spiral cleavage. The optimization of the cleavage pattern on current phylogenetic hypotheses with Nemertodermatida and Acoela as early bilaterian branches is discussed.     

The yeastKluyveromyces africanus nov. spec. and its phylogenetic significance

Summary A new budding yeast species isolated from soil is described. Its outstanding features are, firstly, the formation of asci containing up to sixteen long oval to reniform ascospores and, secondly, a fermentative as well as oxidative metabolism. The assimilation of nitrate is absent and no pseudomycelium is formed. The taxonomic position of the yeast is discussed and it is pointed out that, due to its exceptional ascospore number (1–16), it cannot be classified in any of the existing fermentative genera of theEndomycetaceae (in sensu Lodder et Kreger-van Rij). The reniform shape of its ascospores indicates, however, its close relationship with the multispored genusKluyveromyces, on the one hand, and the newly proposed one to four-spored genusDekkeromyces on the other. The species is provisionally classified as aKluyveromyces species,Kluyveromyces africanus nov. spec., until further information regarding its sexual characteristics becomes available. By virtue of its more or less intermediate ascospore number, it establishes the direct derivation of the genusDekkeromyces fromDipodascus uninucleatus via the multispored yeast genusKluyveromyces.     

The peristomatic structures of Lithobiomorpha (Myriapoda, Chilopoda): comparative morphology and phylogenetic significance

A comparative survey of the epipharynx and hypopharynx of lithobiomorph centipedes by light and scanning electron microscopy examines 18 species that sample the major groups of both families, the Lithobiidae and Henicopidae. Cladistic analysis of 11 characters of the peristomatic structures together with 29 additional morphological characters serves as a basis for interpreting the evolution of the lithobiomorph peristomatic structures. Scutigeromorpha is used for outgroup comparison in the framework of a homology scheme for the basic components of the epi- and hypopharynx. Compared to other chilopods, the monophyly of Lithobiomorpha is supported by a row of distinctive bottle-shaped gland openings at the border between the labral and clypeal parts of the epipharynx, as well as by a distinctive shape of the hypopharynx. Paired rows of elongate spines on the clypeal part of the epipharynx are an apomorphic character of Lithobiidae. The transformation of these spine rows into a few groups of branching spines is characteristic for the Monotarsobius group sensu Verhoeff. Similar groups of branching clypeal spines characterize the Anopsobiinae within Henicopidae, whereas Henicopinae possess a dense cluster of short, simple spines instead. The recently described genus Dzhungaria is resolved closer to Henicopinae than to Anopsobiinae, a hypothesis supported by a field of grooves on the medial labral part of the epipharynx. Monophyly of Henicopidae does not receive unique support from the peristomatic structures although two homoplastic characters contribute to this node; among these, the reduction of a median spine field between clypeal and labral parts of the epipharynx to a narrow transverse band also supports a close relationship between the Ezembius group and Hessebius within Lithobiidae. An Ezembius+Hessebius clade is additionally supported by the absence of a transverse bulge between the clypeal and labral parts of the epipharynx, a character otherwise present in all lithobiomorph species studied so far. Lithobius is resolved as polyphyletic, with different species being most closely related to such genera as Australobius, Hessebius and Pleurolithobius.     

Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov

Sequences of the nuclear encoded small subunit (SSU) rRNA were determined for Pirsonia diadema, P. guinardiae, P. punctigerae, P. verrucosa, P. mucosa and three newly isolated strains 99-1, 99-2, 99-S. Based on phylogenetic analysis all Pirsonia strains, except P. mucosa, clustered together in one clade, most closely related to Hyphochytrium catenoides within the group of stramenopiles. However, P. mucosa was most closely related to Cercomonas sp. SIC 7235 and Heteromita globosa and belongs to the heterogenic group of Cercozoa. In addition to the SSU rDNA sequences, P. mucosa differs from the stramenopile Pirsonia species in some characteristics and was therefore redescribed in this paper as Pseudopirsonia mucosa. The three newly isolated strains 99-1, 99-2, and 99-S differed by 28 bp in their SSU rDNA sequences from their closest neighbour P. diadema and only 1 to 3 bp among themselves. These base differences and a host range similar to P. formosa were sufficient to assign them as new strains of P. formosa.     

Rhododrilus sexpapillatus n.sp. (Oligochaeta: Megascolecidae) from New Zealand

Abstract

A new earthworm species belonging to the acanthodriline genus Rhododrilus is described from the North Island of New Zealand, elevating the generic total (excluding Australian forms) to 30 species. The new taxon forms part of the species-group with incomplete fusion of the male and prostatic terminalia. Its most closely related congener is the geographically proximate R. papaensis. Though exhibiting great heterogeneity, suggestive of polyphyly, the genus remains taxonomically convenient. It probably encompasses convergent forms, the ancestral affinities of which may never be ascertained.     

Redescription of Paralagenophrys singularis (Kellicott) n. comb. (Ciliophora: Peritricha: Lagenophryidae)1

Lagenophrys singularis is removed from Lagenophrys and designated the type species of Paralagenophrys n. g. Compared to members of Lagenophrys, the oral area of P. singularis is radically distorted. Paralagenophrys apparently also lacks second-type division, a special phase of sexual reproduction characteristic of Lagenophrys and associated with its adaptation to symbiotic life on crustaceans. Members of Lagenophrys are obligate ectocommensals of crustaceans. In contrast, P. singularis (Kellicott, 1887) n. comb. occurs most often on the leaves of aquatic vascular plants.     

Fine structure of the pharyngeal apparatus of the pelagosphera larva in Phascolosoma agassizii (Sipuncula) and its phylogenetic significance

Sipuncula is a small taxon of worm-like marine organisms of still uncertain phylogenetic position. Sipunculans are characterized by an unsegmented body composed of a trunk into which the anterior part, the introvert, can be withdrawn. The group has been placed at various positions within Metazoa; currently, it is either seen as sister group of a clade comprising Mollusca and Annelida or as sister to each of these. An in-group position in either Mollusca or Annelida has usually been precluded till now due to the lack of so-called annelid or molluscan “key-characters” such as segmentation and chaetae or the radula. In the development of certain taxa the trochophore stage is followed by a planktonic larva, the pelagosphera, which might exhibit phylogenetically important structures. Among these is the buccal organ, which has been considered homologous either to the ventral pharyngeal organ present in many sedentary polychaetes or to the radular apparatus of molluscs. In the present paper, the ventral pharynx of the pelagosphera larva of Phascolosoma agassizii is investigated by transmission electron microscopy. The pharynx comprises dorsolateral ciliary folds, a muscle bulb formed by transverse muscle fibres with large intercellular spaces, and an investing muscle. A tongue-like organ is lacking. These results show great structural correspondences to the ventral pharynx of polychaetes, especially to that of the flabelligerid Diplocirrus longisetosus. In contrast, there are no signs of structural similarities to the corresponding structures of molluscs. Thus evidence increases that Sipuncula are closely related to annelids; moreover, an in-group position of Sipuncula within Annelida, as suggested by recent molecular studies, is not precluded by the present data. Instead these studies find additional support. Hence the lack of segmentation and chitinous chaetae in Sipuncula would be a secondary rather than a primary situation, as has recently been shown for Echiura and Pogonophora.