Zorotypus Hubbardi Research Articles

Winter Occurrence of Zorotypus Hubbardi (Zoraptera) in Tippecanoe County, Indiana

Winter Occurrence of Zorotypus Hubbardi (Zoraptera) in Tippecanoe County, Indiana

The morphology and ultrastructure of salivary glands of Zoraptera (Insecta)

The salivary glands of two species of Zoraptera, Zorotypus caudelli and Zorotypus hubbardi, were examined and documented mainly using transmission electron microscopy (TEM). The results obtained for males and females of the two species are compared and functional aspects related to ultrastructural features are discussed. The salivary glands are divided into two regions: the secretory cell region and the long efferent duct, the latter with its distal end opening in the salivarium below the hypopharyngeal base. The secretory region consists of a complex of secretory cells provided with microvillated cavities connected by short ectodermal ducts to large ones, which are connected with the long efferent duct. The secretory cell cytoplasm contains a large system of rough endoplasmic reticulum and Golgi apparatus producing numerous dense secretions. The cells of the efferent duct, characterized by reduced cytoplasm and the presence of long membrane infoldings associated with mitochondria, are possibly involved in fluid uptaking from the duct lumen.

The morphology of the eggs of three species of Zoraptera (Insecta)

The egg structure of Zorotypus magnicaudelli, Zorotypus hubbardi and Zorotypus impolitus was examined and described in detail. Major characteristics of zorapteran eggs previously reported were confirmed in these species, with the partial exception of Z. impolitus: 1) a pair of micropyles at the equator of the egg's ventral side, 2) a honeycomb pattern on the egg surface, 3) a two-layered chorion, 4) micropylar canals running laterally, 5) a flap covering the inner opening of the micropylar canal and 6) no region specialized for hatching. These features are probably part of the groundplan of the order. Three groups (A–C) and two subgroups (A1 and A2) of Zoraptera can be distinguished based on characters of the reproductive apparatus including eggs. However, information for more species is needed for a reliable interpretation of the complex and apparently fast evolving character system. The egg of Z. impolitus presumably shows apomorphic characteristics not occurring in other species, a chorion without layered construction and polygonal surface compartments with different sculptures on the dorsal and ventral sides of the egg. Another feature found in this species, distinct enlargement of the micropyles, is also found in Z. hubbardi. The increased micropylar size is likely correlated with the giant spermatozoa produced by males of these two species. These two features combined with the large size of the spermatheca are arguably a complex synapomorphy of Z. hubbardi and Z. impolitus. The phylogenetic placement of Zoraptera is discussed based on the egg structure. A clade of Zoraptera + Eukinolabia appears most plausible, but the issue remains an open question.

Antennal heart morphology supports relationship of Zoraptera with polyneopteran insects

AbstractThe antennal hearts of the zorapteran Zorotypus hubbardi and of two psocopteran species (Caecilius sp., Embidopsocus sp.) are described in detail and compared to those of other insects. In Zorotypus, the ampullae of this organ are located dorsally of the antennal base. They are attached to the frontal cuticle of the head capsule and laterally suspended by two delicate bands of connective tissue. The associated muscles comprise a well‐developed M. interampullaris and a M. ampulloaortica, which together act as dilators of the ampullae. The connected antennal vessel has a very thin wall and is uniform along its entire length. In the two studied psocopterans the ampullae are likewise connected to the head capsule and have two additional elastic bands. In Caecilius sp. the anterior band is muscular, while in Embidopsocus sp. it is the posterior one. The psocopteran antennal hearts have no additional musculature. Antennal hearts with a musculature configuration resembling that of Zoraptera are known only from Dictyoptera, Phasmatodea and some orthopterans. This condition thus might be a synapomorphy of a polyneopteran subgroup including Zoraptera.

Comparative morphology of spermatozoa and reproductive systems of zorapteran species from different world regions (Insecta, Zoraptera)

The male and female reproductive apparatus of Zorotypus magnicaudelli (Malaysia), Zorotypus huxleyi (Ecuador) and Zorotypus weidneri (Brazil) were examined and documented in detail. The genital apparatus and sperm of the three species show only minor differences. The testes are larger in Z. magnicaudelli. Z. huxleyi lacks the helical appendage in the accessory glands. A long cuticular flagellum is present in Z. magnicaudelli and in the previously studied Zorotypus caudelli like in several other species, whereas it is absent in Z. weidneri, Z. huxleyi, Zorotypus hubbardi, Zorotypus impolitus and Zorotypus guineensis. Characteristic features of the very similar sperm are the presence of: a) two dense arches above the axoneme; b) a 9 + 9+2 axoneme with detached subtubules A and B of doublets 1 and 6; c) the axonemal end degenerating with enlarging accessory tubules; d) accessory tubules with 17 protofilaments; e) three accessory bodies beneath the axoneme; and f) two mitochondrial derivatives of equal shape. The first characteristic (a) is unknown outside of Zoraptera and possibly autapomorphic. The sperm structure differs distinctly in Z. impolitus and Z. hubbardi, which produce giant sperm and possess a huge spermatheca. The presence of the same sperm type in species either provided with a sclerotized coiled flagellum in males or lacking this structure indicates that a different organization of the genital apparatus does not necessarily affect the sperm structure. The flagellum and its pouch has probably evolved within Zoraptera, but it cannot be excluded that it is a groundplan feature and was reduced several times. The fossil evidence and our findings suggest that distinct modifications in the genital apparatus occurred before the fragmentation of the Gondwanan landmass in the middle Cretaceous.

The male and female reproductive systems of Zorotypus hubbardi Caudell, 1918 (Zoraptera)

Here we present an ultrastructural study of the male and female reproductive systems of Zorotypus hubbardi and compare the findings to those presented in an earlier study. The male reproductive system consists of small testes and thin and short deferent ducts opening into a huge seminal vesicle. At the end of the deferent duct a wiredrawer structure is present which initiates the spermatophore formation. A long ejaculatory duct, originating from the seminal vesicle, receives the secretions of three accessory glands. The copulatory organ is a relatively stout structure consisting of two cuticular claspers connected to a ventral sclerite. The testes contain very large and few germ cells (32 sperm in each cyst) which give rise to large sperm characterized by two giant mitochondrial derivatives, two large accessory bodies, and an axoneme with accessory tubules with 17 protofilaments in their tubular wall. In the seminal vesicle the sperm are joined by a secretion to form an elongate spermatophore. The female system consists of panoistic ovarioles, two lateral oviducts, and a common oviduct which receives the spermathecal duct of a huge spermathecal sac in the terminal part of the vagina. The duct is an anterior prolongation of the sac. Its distal part turns back twisting around its proximal portion. At this level a conspicuous muscle layer gives rise to a valve. The bent spermatophore is hosted in the spermathecal sac, with the sperm heads placed in the proximal part of the spermathecal duct. The opening of the duct is close to the female genital opening. The reproductive systems of Zorotypus caudelli and Z. hubbardi, apart from a distinctly different general organization, also have a different sperm structure: those of the former species are free long-moving cells, while the sperm of Z. hubbardi are giant cells joined in a spermatophore. This allows to hypothesize and discuss a different reproductive behaviour in the two species: monandric in Z. hubbardi and polyandric in Z. caudelli. Apparently different forms of selection have resulted in a very uniform general morphology in Zoraptera, and in highly divergent features related to the reproductive system. The presence of 17 protofilaments in the accessory microtubules of the flagellar axoneme is a potential synapomorphy of Zoraptera and Phasmatodea.

The fine structure of the female reproductive system of Zorotypus caudelli Karny (Zoraptera)

The general structure of the female genital system of Zorotypus caudelli is described. The ovarioles are of the panoistic type. Due to the reduction of the envelope (tunica externa) the ovarioles are in direct contact with the hemolymph like in some other insect groups, Plecoptera included. The calices are much larger in Z. caudelli then in Zorotypus hubbardi and their epithelial cells produce large amounts of secretions, probably protecting the surface of the eggs deposited on the substrate. Eggs taken from the calyx bear a series of long fringes, which are missing in the eggs found in the ovariole, and in other zorapteran species. The long sperm of Z. caudelli and the long spermathecal duct are likely related to a sexual isolating mechanism (cryptic female choice), impeding female re-mating. The apical receptacle and the spermathecal duct - both of ectodermal origin - consist of three cell types. In addition to the cells beneath the cuticle lining the lumen, two other cell types are visible: secretory and canal cells. The cytoplasm of the former is rich in rough endoplasmic reticulum cisterns and Golgi complexes, which produce numerous discrete dense secretory bodies. These products are released into the receiving canal crossing the extracellular cavity of secretory cells, extending over a series of long microvilli. The secretion is transported towards the lumen of the apical receptacle of the spermatheca or to that of the spermathecal duct by a connecting canal formed by the canal cells. It is enriched by material produced by the slender canal cells. Before mating, the sperm cells are enveloped by a thick glycocalyx produced at the level of the male accessory glands, but it is absent when they have reached the apical receptacle, and also in the spermathecal duct lumen. It is likely removed by secretions of the spermatheca. The eggs are fertilized at the level of the common oviduct where the spermathecal duct opens. Two micropyles at the dorsal side of the equator level possibly facilitate fertilization. The presence of these two micropyles is a presumably derived feature shared with Phasmatodea. The fine structure of the female reproductive system of Z. caudelli does not allow to assess the phylogenetic position at the present stage of knowledge. The enlarged calyx and the temporary presence of long fringes on the eggs are potential autapomorphies of Z. caudelli or may indicate relationships with other Zorotypus species.

The male reproductive system of Zorotypus caudelli Karny (Zoraptera): Sperm structure and spermiogenesis

Considering the overall uniformity of the morphology of Zoraptera, the structural diversity of the male genital system is remarkable. Structures related to the male reproductive system of Zorotypus caudelli differ profoundly from those of Zorotypus hubbardi. The testes are elongated rather than spherical, the seminal vesicle is apparently absent, and the deferent ducts are very long. A feature shared by these two species and other zorapterans examined is that the two accessory glands are closely adherent to each other and form a single large structure, from which the ejaculatory duct originates. This is a potential zorapteran autapomorphy. Another feature possibly present in the groundplan of the order is the strong elongation of the sperm cells. This may be connected with a reproductive strategy of males trying to avoid re-mating of females with other males after the first copulation. The extremely long and coiled spermathecal duct of Z. caudelli and other zorapteran species is possibly correlated with the sperm elongation, and both features combined may result in a sexual isolating mechanism. The short duration of mating of Zorotypus barberi and Zorotypus gurneyi suggests that the male introduces sperm into the female tract up to the opening of the spermathecal duct using their long coiled aedeagus. A thick glycocalyx around the sperm in the distal part of the deferent ducts probably protects the sperm cells during their forward progression towards the long spermathecal duct, and is removed when they reach the apical receptacle. The spermatogenesis of Z. caudelli follows a pattern commonly found in insects, but differs distinctly from that of Z. hubbardi in the number of spermatids in each sperm cyst. An unusual and possibly autapomorphic feature of Z. caudelli is a disconnection of sub-tubules A and B at the level of microtubule doublets 1 and 6 of the mature sperm cells. It is conceivable that this results in a shorter period of sperm motility. The character combination found in different zorapteran species supports the view that the sperm, a very compact functional unit, does not evolve as a unit, but like in other more complex body regions, sperm components can also be modified independently from each other. This results in different mosaic patterns of plesiomorphic and derived features in a very compact entity in different species of the very small and otherwise uniform order Zoraptera. In Z. caudelli, for instance, the bi-layered acrosome and small accessory bodies are plesiomorphic states among several others, whereas the mitochondrial derivatives and the elongate nucleus are apparently derived conditions. Other combinations likely occur in other zorapteran species. Only few but noteworthy sperm characters indicate possible phylogenetic affinities of Zoraptera. A possible synapomorphic feature, the presence of dense laminae radiating in a cartwheel array between neighbouring centriolar triplets, is shared with Phasmatodea and Embioptera. Another potential synapomorphy shared with Phasmatodea is the presence of 17 protofilaments in the tubular wall of the outer accessory microtubules.

The genital morphology of Zorotypus hubbardi Caudell, 1918 (Insecta: Zoraptera: Zorotypidae)

The internal and external genitalia of both sexes of Zorotypus hubbardi Caudell 1918 were examined. A detailed description is provided, especially for the male genitalia. The results were compared with the conditions in potentially related neopteran groups. Most features of the internal genitalia of both sexes are plesiomorphic. Putative autapomorphies are: fusion of the distal parts of the vasa deferentia, division of the ductus ejaculatorius (de) into two sections by a distinct circular furrow, dorso-median processes on tergites VIII–X, an asymmetric aedoeagus with a cryptic slit-like phallotrema, reduction of the right outer paramere, the specific asymmetric shape of the endophallus with three conspicuous pouches, the endophallic sclerites scl1–scl6 and their specific arrangement, the specific arrangement of the endophallic muscularis and the unpaired genital muscles m2, m4, m5, m6 and m7. These features cannot be regarded as autapomorphies of the whole order Zoraptera with reliability, as the morphology of the external male genitalia seems to be highly variable within the genus Zorotypus and the intra-generic relationships are poorly resolved. Potential synapomorphies were found with several neopteran groups under comparison: with Embiidina a strengthened muscularis surrounding the de, reduction of the ovipositor and a shortened tergite IX, with Psocoptera the occurance of dense sperm bundles and with Hemiptera a strengthened muscularis of the de. No synapomorphies were found with Dictyoptera. Homologies of the muscles m1 and m3 found in Z. hubbardi with some genital muscles in Dictyoptera and Psocoptera are highly ambiguous.

The thorax of Zorotypus (Hexapoda, Zoraptera) and a new nomenclature for the musculature of Neoptera

External and internal features of the thorax of alate and wingless morphs of Zorotypus hubbardi and Z. weidneri were examined and described in detail. Three-dimensional computer reconstructions were carried out based on microtome section series. Skeletal structures are less sclerotised in the wingless specimens and the limits of sclerites are indistinct. The alate morphs are almost exclusively characterised by plesiomorphic features and their thoracic morphology is probably close to the neopteran groundplan. The skeletal structures are very similar to the condition found in Plecoptera and the muscle system comprises nearly the maximum number known in representatives of Neoptera. Based on the morphological investigation of Zorotypus and comparisons with data for other taxa from the literature, a new consistent nomenclature for the thoracic muscular system of Neoptera is proposed. The few derived features found in the thoracic skeleto-muscular apparatus of Zorotypus are mostly autapomorphic. The obtained data do not clearly indicate the systematic placement of the order. However, the arguments for a close relationship with Endopterygota or Dictyoptera, respectively, are refuted.

Karyotype, reproductive organs, and pattern of gametogenesis in Zorotypus hubbardi Caudell (Insecta: Zoraptera, Zorotypidae), with discussion on relationships of the order

For the first time, the karyotype is described in a representative of the order Zoraptera. Zorotypus hubbardi Caudell (Zorotypidae) have holokinetic chromosomes and male karotype of 2n = 38 (36 + neo-XY). Males possess two follicles in each testis and females have six panoistic ovarioles in each ovary. Oogenesis and, more closely, spermato genesis, including meiosis and sperm formation, have been studied. Based on the presence of panoistic ovaries and holokinetic chromosomes, Crampton's hypothesis that Zoraptera represent a group of Polyneoptera nearest to the origin of Paraneoptera is considered the most plausible.

The Distribution of Zorotypus hubbardi (Zoraptera)

The known range of Zorotypus hubbardi Caudell, originally thought restricted to subtropical areas, has been greatly expanded northward in recent years and now extends beyond the 41st parallel. Colonies, most of which probably overwinter in decaying sawdust piles, have been found throughout the deciduous forest region as far north as Iowa and Pennsylvania. Wind-borne, fertilized, alate females are regarded as responsible for the range extension of this species. New locality records and a distribution map are given, together with notes on the biology of Z. hubbardi .