Homology of the wing base sclerites in Ephemeroptera (Insecta: Pterygota) - a reply to Willkommen and Hörnschemeyer

We revised the homology of wing base structure in Ephemeroptera (Insecta: Pterygota) proposed by Willkommen and Hörnschemeyer in a recent issue of Arthropod Structure and Development. The first free sclerite (s1) in Ephemeroptera should be homologized with a part of the first axillary sclerite (1Ax) of Neoptera, together with the second free sclerite, whereas the authors recognized s1 as a detached part of the anterior notal wing process. The fifth free sclerite of Ephemeroptera should be homologized with the median notal wing process of Neoptera, rather than it being homologous with a part of 1Ax in Neoptera, as the authors postulated. Hypothesized secondary fusion of the axillary sclerites in Ephemeroptera and Odonata proposed by the authors is premature, because the basal phylogeny of Pterygota is still poorly understood, and an alternative interpretation of morphological evolution (i.e., that undifferentiated axillary sclerites represent the ground plan of Pterygota) can also be drawn from the Ephemeroptera + Neoptera hypothesis.     

Origin and evolution of insect wings and their relation to metamorphosis,as documented by the fossil record

In contemporary entomology the morphological characters of insects are not always treated according to their phylogenetic rank. Fossil evidence often gives clues for different interpretations. All primitive Paleozoic pterygote nymphs are now known to have had articulated, freely movable wings reinforced by tubular veins. This suggests that the wings of early Pterygota were engaged in flapping movements, that the immobilized, fixed, veinless wing pads of Recent nymphs have resulted from a later adaptation affecting only juveniles, and that the paranotal theory of wing origin is not valid. The wings of Paleozoic nymphs were curved backwards in Paleoptera and were flexed backwards at will in Neoptera, in both to reduce resistance during forward movement. Therefore, the fixed oblique-backwards position of wing pads in all modern nymphs is secondary and is not homologous in Paleoptera and Neoptera. Primitive Paleozoic nymphs had articulated and movable prothoracic wings which became in some modern insects transformed into prothoracic lobes and shields. The nine pairs of abdominal gillplates of Paleozoic mayfly nymphs have a venation pattern, position, and development comparable to that in thoracic wings, to which they are serially homologous. Vestigial equivalents of wings and legs were present in the abdomen of all primitive Paleoptera and primitive Neoptera. The ontogenetic development of Paleozoic nymphs was confluent, with many nymphal and subimaginal instars, and the metamorphic instar was missing. The metamorphic instar originated by the merging together of several instars of old nymphs; it occurred in most orders only after the Paleozoic, separately and in parallel in all modern major lineages (at least twice in Paleoptera, in Ephemeroptera and Odonata; separately in hemipteroid, blattoid, orthopteroid, and plecopteroid lineages of exopterygote Neoptera; and once only in Endopterygota). Endopterygota evolved from ametabolous, not from hemimetabolous, exopterygote Neoptera. The full primitive wing venation consists of six symmetrical pairs of veins; in each pair, the first branch is always convex and the second always concave; therefore costa, subcosta, radius, media, cubitus, and anal are all primitively composed of two separate branches. Each pair arises from a single veinal base formed from a sclerotized blood sinus. In the most primitive wings the circulatory system was as follows: the costa did not encircle the wing, the axillary cord was missing, and the blood pulsed in and out of each of the six primary, convex-concave vein pair systems through the six basal blood sinuses. This type of circulation is found as an archaic feature in modern mayflies. Wing corrugation first appeared in preflight wings, and hence is considered primitive for early (paleopterous) Pterygota. Somewhat leveled corrugation of the central wing veins is primitive for Neoptera. Leveled corrugation in some modern Ephemeroptera, as well as accentuated corrugation in higher Neoptera, are both derived characters. The wing tracheation of Recent Ephemeroptera is not fully homologous to that of other insects and represents a more primitive, segmental stage of tracheal system. Morphology of an ancient articular region in Palaeodictyoptera shows that the primitive pterygote wing hinge in its simplest form was straight and composed of two separate but adjoining morphological units: the tergal, formed by the tegula and axillaries; and the alar, formed by six sclerotized blood sinuses, the basivenales. The tergal sclerites were derived from the tergum as follows: the lateral part of the tergum became incised into five lobes; the prealare, suralare, median lobe, postmedian lobe and posterior notal wing process. From the tips of these lobes, five slanted tergal sclerites separated along the deep paranotal sulcus: the tegula, first axillary, second axillary, median sclerite, and third axillary. Primitively, all pteralia were arranged in two parallel series on both sides of the hinge. In Paleoptera, the series stayed more or less straight; in Neoptera, the series became V-shaped. Pteralia in Paleoptera and Neoptera have been homologized on the basis of the fossil record. A differential diagnosis between Paleoptera and Neoptera is given. Fossil evidence indicates that the major steps in evolution, which led to the origin first of Pterygota, then of Neoptera and Endopterygota, were triggered by the origin and the diversification of flight apparatus. It is believed here that all above mentioned major events in pterygote evolution occurred first in the immature stages.     

The Palaeoptera Problem: Basal Pterygote Phylogeny Inferred from 18S and 28S rDNA Sequences

Monophyly of the pterygote insects is generally accepted, but the relationships among the three basal branches (Odonata, Ephemeroptera and Neoptera) remain controversial. The traditional view, to separate the pterygote insects in Palaeoptera (Odonata + Ephemeroptera) and Neoptera, based on the ability or inability to fold the wings over the abdomen, has been questioned. Various authors have used different sets of morphological characters in support of all three possible arrangements of the basal pterygote branches. We sequenced 18S and 28S rDNA from 18 species of Odonata, 8 species of Ephemeroptera, 2 species of Neoptera, and 1 species of Archaeognatha in our study. The new sequences, in combination with sequences from GenBank, have been used in a parsimony jackknife analysis resulting in strong support for a monophyletic Palaeoptera. Morphological evidence and the phylogenetic implications for understanding the origin of insect flight are discussed.     

Morphology of the elytral base sclerites

The elytral base sclerites (= sclerites located at the articular region between the forewing and thorax in Coleoptera) of selected taxa were examined and homologized. Although the elytral base sclerites are highly modified compared to the wing base sclerites of the other neopterans, they can be homologized by using the conservative wing flapping and folding lines as landmarks. A reduction of the first axillary sclerite was identified as a general trend of the elytral base sclerites, although the sclerite usually has a very important function to mediate flight power from the notum to the wing. This result indicates that the functional constraint against the basal sclerites is relaxed because of the lack of an ability to produce flight power by elytra. In contrast, the elytral folding system formed by the basal sclerites is well retained, which probably occurs because proper wing folding is a key for the shelter function of the elytra. The elytral base sclerites apparently contain more homoplasies than the serially homologous hindwing base sclerites of Coleoptera, which suggests that the structure is less useful for higher-level systematics. However, the faster evolutionary rate of the elytral base sclerites suggests there is potential for studying the lower-level phylogeny of Coleoptera.     

The wing base of the palaeodictyopteran genus Dunbaria Tillyard: Where are we now?

The structure of insect wing articulation is considered as reliable source of high level characters for phylogenetic analyses. However, the correct identification of homologous structures among the main groups of Pterygota is a hotly debated issue. Therefore, the reconstruction of the wing bases in Paleozoic extinct relatives is of great interest, but at the same time it should be treated with extreme caution due to distortions caused by taphonomic effects. The present study is focused on the wing base in Dunbaria (Spilapteridae). The articulation in Dunbaria quinquefasciata is mainly formed by a prominent upright axillary plate while the humeral plate is markedly reduced. Due to unique preservation of surface relief of the axillary plate, its composition shows a detailed pattern of three fused axillary sclerites and presumable position of the sclerite 3Ax. The obtained structures were compared among Spilapteridae and to other palaeodictyopterans Ostrava nigra (Homoiopteridae) and Namuroningxia elegans (Namuroningxiidae). The comparative study uncovered two patterns of 3Ax in Dunbaria and Namuroningxia, which correspond to their different suprafamilial classification. In contrast to previous studies these new results reveal the homologous structural elements in the wing base between Paleozoic Palaeodictyoptera and their extant relatives of Ephemeroptera, Odonata and Neoptera.     

现存蜉蝣翅基纵脉走向及愈合模式(昆虫纲：蜉蝣目)

有翅昆虫翅基纵脉的走向及愈合模式在系统发育重建中占有重要地位。然而,现存蜉蝣翅基纵脉的走向及愈合状况在大部分种类变化极大,无法推测其原始状况,只在极少数种类保留有部分可见残迹。中国拟短丝蜉Siphluriscus chinensis的翅基保留有独立的亚前缘脉弓、部分中脉M和肘脉Cu主干以及前中脉MA及径分脉Rs的走向痕迹。据此并结合红斑蜉Ephemera rufomaculata 和大网脉蜉Chromarcys magnifica翅基的相关特征,本文提出了蜉蝣目主要纵脉基部走向及愈合的基本模式,其要点有：中脉主干在基部与径脉主干独自发出后先接近或愈合后又分离、它们各自分成两支后的前中脉及径分脉又先愈合再分离、肘脉始终独立。这种中脉与径脉先接近或愈合后分离的模式非常接近新翅类的情况而与蜻蜓很不相同(在蜻蜓,中脉与肘脉在基部愈合) 。亚前缘脉弓的作用相信是加强了因翅基骨板发达而相互远离的纵脉间的连结作用。这个假说也可以来解释蜻蜓复杂脉相的形成原因。     

A revised interpretation of the wing base structure in Odonata

Abstract Homology of the wing base structure in the Odonata is highly controversial, and many different interpretations of homology have been proposed. In extreme cases, two independent origins of insect wings have been suggested, based on comparative morphology between the odonate and other pterygote wing bases. Difficulties in establishing homology of the wing base structures between Odonata and other Pterygota result mainly from their extreme differences in morphology and function. In the present paper, we establish homology of the wing base structures between Neoptera, Ephemeroptera and Odonata using highly conservative and unambiguously identifiable characters (the basal wing hinge and subcostal veins) as principal landmarks. Homology of the odonate wing base structure with those of Ephemeroptera and Neoptera can be identified reliably. Based on this interpretation, the ancestral condition of the insect wing base structure is discussed.     

Morphology and evolution of the wing bullae in South American Leptophlebiidae (Ephemeroptera)

Insects were the first animals to take to the skies, and have been flying for over 320 million years. The order Ephemeroptera is, or at least is part of, the most early-diverging lineage of extant winged insects. The extant species present a very short adult life span, mainly dedicated to reproduction and dispersal of eggs. Mating and egg-laying behavior depend on flight. Wings are structures to fly and as such face a number of physical and physiological challenges. The convex curvature along the anterior–posterior axis of the wing generates a camber that must be carefully regulated. One of the most interesting ways of wing bending is provided by the bullae, which have been defined as short sections of flexible chitin, where the flexion lines cross veins. Although the bullae have been frequently used as taxonomic characters, there is no study focused on their morphology, although their prevalence on the wings of mayflies strongly suggests a role in flight. In order to identify evolutionary trends of these structures within Ephemeroptera, we constructed a matrix with comparative anatomy data of the bullae from whole mounts of the wings of 300 specimens belonging to 70 species of several mayfly families, as well as scanning microscopy samples of selected specimens. We also surveyed the number of bullae and their distribution in the wings of the different species within the South American Leptophlebiidae clade. We optimized the characters onto the latest published phylogeny for Leptophlebiidae.     

The complete mitochondrial genome of Parafronurus youi (Insecta: Ephemeroptera) and phylogenetic position of the Ephemeroptera

The first complete mitochondrial genome of a mayfly, Parafronurus youi (Arthropoda: Insecta: Pterygota: Ephemeroptera: Heptageniidae), was sequenced using a long PCR-based approach. The genome is a circular molecule of 15,481 bp in length, and encodes the set of 38 genes. Among them, 37 genes are found in other conservative insect mitochondrial genomes, and the 38(th) unique gene is trnM-like (trnM2). The duplication-random loss model can be used to explain one of the translocations at least. The A+T content of the control region is 57%, the lowest proportion detected so far in Hexapoda. Based on the nucleotide dataset and the corresponding amino acid dataset of 12 protein-coding genes, Bayesian inference and maximum likelihood analyses yielded stable support for the relationship of the three basal clades of winged insects as Ephemeroptera+(Odonata+Neoptera).     

部分具翅昆虫后胸足基骨片的分化与系统发育

从12目具翅昆虫中选出16个代表种,对其后足基骨片的形态特征在不同类群中的衍变进行分析比较,据此构建反映下列初步进化关系的系统树:[Ephemeroptera+(Odonata+Neoptera)]+[Plecoptera+(Megaloptera+Neuroptera+(Orthoptera+(Hemiptera+(...     

三尾类蜉蝣成熟稚虫的翅芽脉相(蜉蝣目)(英语)

本文记述了三尾类蜉蝣Ephemeropsis trisetalis稚虫的脉相和翅关节区特征为化石昆虫保存史上罕见材料,脉相中显出颇大的径脉区和前缘区十分相似于某些原始的古生代蜉蝣,或许可以提示发达的径脉区和前缘脉区是蜉蝣翅进化史中的初期特征.再者,现代蜉蝣的翅关节区退化,一般由一组不发达,分化很弱的骨板和肩板组成;这个化石种的翅关节区具发达的骨板和肩板似指示现化蜉蝣翅关节区退化是后生获得的性状.     

The problem with "the Paleoptera Problem:" sense and sensitivity

While the monophyly of winged insects (Pterygota) is well supported, phylogenetic relationships among the most basal extant pterygote lineages are problematic. Ephemeroptera (mayflies) and Odonata (dragonflies) represent the two most basal extant lineages of winged insects, and determining their relationship with regard to Neoptera (remaining winged insects) is a critical step toward understanding insect diversification. A recent molecular analysis concluded that Paleoptera (Odonata Ephemeroptera) is monophyletic. However, we demonstrate that this result is supported only under a narrow range of alignment parameters. We have further tested the monophyly of Paleoptera using additional sequence data from 18SrDNA, 28S rDNA, and Histone 3 for a broader selection of taxa and a wider range of analytical methodologies. Our results suggest that the current suite of molecular data ambiguously resolve the three basal winged insect lineages and do not provide independent confirmation of Odonata + Neoptera as supported via morphological data.     

The morphology and terminology of the hindwing articulation and wing base of the Coleoptera, with specific reference to the Scarabaeoidea

Abstract. Characters of the hindwing articulation and wing base are important for contributing to the solution of phylogenetic and systematic problems in the Coleoptera. In the Scarabaeoidea morphological terms proposed by previous authors do not cover many structures in sufficient detail and additional terms are needed to describe and utilize all characters used in systematic considerations; these can be used for all Coleoptera.
In this paper we identify new structures, the first basal plate and the second basal plate (two subdivisions of the coleopteran wing base), name the various yokes, braces and reinforcements found on them and propose names for various projections, lobes, indentations and embayments on the axillary sclerites (first axillary, head, neck and tail; second axillary, arm and body; third axillary, prong; basalare).     

THE VENATION OF THE MATURE NYMPH WING PAD OF EPHEMEROPSIS TRISETALIS EICHWALD (EPHEMEROPTERA: HEXAGENITIDAE)

Abstract  The complete mature nymph wing pad with distinct venation has been collected from Jiuquan Basin, Northwest China, which is almost without precedent in the fossil history of insect. The venation with large radial and costal fields is considered as archaic feature which very probably represents the primitive stage in the evolution of Ephemeroptera. Furthermore, as compared with the modern adult wing, the stronger articular sclerites in the fossil nymphal wing pad of Ephemeropsis trisetalis probably shows that the reduction of the articulation in modern mayfly wing is a secondarily acquired character.     

"古翅类"系统发育关系研究进展(昆虫纲,有翅类)

古翅类的系统发育问题是六足总纲中有争议的热点问题之一。对现存古翅类(孵蝣目 蜻蜒目)与新翅类之间的系统发育关系有3种主要观点：古翅类(＝蜉蝣目 蜻蜒目) 新翅类,蜉蝣目 (蜻蜒目 新翅类),蜻蜒目 (蜉蝣目 新翅类)。第1种观点得到化石、形态和部分基因证据支持,第2种观点得到较多形态特征支持,支持第3种观点的证据较少。这一问题的解决有赖于更多昆虫种类、化石以及分子证据的发现和研究。     

Shifts in hexapod diversification and what Haldane could have said

Data on species richness and taxon age are assembled for the extant hexapod orders (insects and their six-legged relatives). Coupled with estimates of phylogenetic relatedness, and simple statistical null models, these data are used to locate where, on the hexapod tree, significant changes in the rate of cladogenesis (speciation-minus-extinction rate) have occurred. Significant differences are found between many successive pairs of sister taxa near the base of the hexapod tree, all of which are attributable to a shift in diversification rate after the origin of the Neoptera (insects with wing flexion) and before the origin of the Holometabola (insects with complete metamorphosis). No other shifts are identifiable amongst supraordinal taxa. Whilst the Coleoptera have probably diversified faster than either of their putative sister lineages, they do not stand out relative to other closely related clades. These results suggest that any Creator had a fondness for a much more inclusive clade than the Coleoptera, definitely as large as the Eumetabola (Holometabola plus bugs and their relatives), and possibly as large as the entire Neoptera. Simultaneous, hence probable causative events are discussed, of which the origin of wing flexion has been the focus of much attention.     

基于四种金龟的昆虫后翅关节骨片三维形态复杂性研究

【目的】昆虫的翅非常精巧与灵活,翅脉及翅关节的形态及功能长久以来受到众多领域科学家的广泛关注。由于历史条件的限制,昆虫翅的研究主要集中在翅脉,即使少量的有关翅关节形态的研究也主要是停留在二维形态数据分析的层面上。更重要的是,各骨片内部形态结构还未见报道。本研究的目的就是为了重建翅关节骨片内部和外部复杂的三维形态结构,全面呈现利用传统形态学方法无法获得的形态学信息,进而深入探究昆虫翅的形态与功能的关系。【方法】本文利用显微CT对鞘翅目4种金龟进行了扫描,通过计算机三维重建技术,对折叠和展开状态时后翅关节各个骨片（第1, 2和3腋片及中片）的内部和外部的三维形态进行研究,展示和分析昆虫翅关节内部与外部形态结构和空间运动的复杂性。【结果】翅关节骨片的三维重建模型及虚拟切面图展示了其复杂的外部形态,主要表现在表面曲率的不均匀变化和部分结构的互相遮挡两个方面。前者主要表现骨片表面具有突起、沟槽、弯折以及外长物等。后者指各骨片均呈现了不同程度的弯折,有的弯折还会互相接触,最终形成筒状结构,这样不可避免造成部分结构被遮挡或包裹。三维重建模型的断层图显示了翅关节骨片并非是实心的结构,而是分为两层：靠近表皮的为高度骨化的外骨骼,而靠近骨片核心则为疏松的类似海绵状结构。本文还展示了各个骨片在后翅折叠状和展开状态下的空间位置,并对所研究的4个科的翅关节骨片的三维形态进行了比较。【结论】翅关节骨片具有复杂的内部和外部形态结构。关节骨片的内部海绵结构和外层强烈骨化的双层结构,可能与其尽量减小骨片的重量和节约运动能量,同时又尽量保持骨片的刚性结构的形态适应策略有关。此类形态适应在材料学、空气动力学等领域具有重要的仿生学意义。     

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 sense of smell in Odonata: An electrophysiological screening

Volatile chemicals mediate a great range of intra- and interspecific signalling and information in insects. Olfaction has been widely investigated mostly in Neoptera while the knowledge of this sense in most basal insects such as Paleoptera (Odonata and Ephemeroptera) is still poor. In the present study we show the results of an electrophysiological screening on two model species, Libellula depressa (Libellulidae) and Ischnura elegans (Coenagrionidae), representatives of the two Odonata suborders Anisoptera and Zygoptera, with the aim to deep the knowledge on the sense of smell of this insect order. The antennal olfactory sensory neurons (OSNs) of these two species responded to the same 22 compounds (out of 48 chemicals belonging to different functional groups) encompassing mostly amines, carboxylic acids or aldehydes and belonging to green leaf volatiles, vertebrate related volatiles and volatiles emitted by standing waters bacteria. The properties of Odonata OSNs are very similar to those of ionotropic receptors (IRs) expressing OSNs in other insects.