Distal leg structures of the Aculeata (Hymenoptera): A comparative evolutionary study of Sceliphron (Sphecidae) and Formica (Formicidae)

The distal parts of the legs of Sceliphron caementarium (Sphecidae) and Formica rufa (Formicidae) are documented and discussed with respect to phylogenetic and functional aspects. The prolegs of Hymenoptera offer an array of evolutionary novelties, mainly linked with two functional syndromes, walking efficiently on different substrates and cleaning the body surface. The protibial-probasitarsomeral cleaning device is almost always well-developed. A complex evolutionary innovation is a triple set of tarsal and pretarsal attachment devices, including tarsal plantulae, probasitarsomeral spatulate setae, and an arolium with an internal spring-like arcus, a dorsal manubrium, and a ventral planta. The probasitarsal adhesive sole and a complex arolium are almost always preserved, whereas the plantulae are often missing. Sceliphron has retained most hymenopteran ground plan features of the legs, and also Formica, even though the adhesive apparatus of Formicidae shows some modifications, likely linked to ground-oriented habits of most ants. Plantulae are always absent in extant ants, and the arolium is often reduced in size, and sometimes vestigial. The arolium contains resilin in both examined species. Additionally, resilin enriched regions are also present in the antenna cleaners of both species, although they differ in which of the involved structures is more flexible, the calcar in Sceliphron and the basitarsal comb in Formica. Functionally, the hymenopteran distal leg combines (a) interlocking mechanisms (claws, spine-like setae) and (b) adhesion mechanisms (plantulae, arolium). On rough substrate, claws and spine-like setae interlock with asperities and secure a firm grip, whereas the unfolding arolium generates adhesive contact on smooth surfaces. Differences of the folded arolium of Sceliphron and Formica probably correlate with differences in the mechanism of folding/unfolding.     

Design of insect unguitractor apparatus

The structure of the unguitractor system of insect legs was studied using scanning and transmission electron microscopy. On the base of serial semithin sections, the 3-D reconstruction of structures of the terminal tarsomere was obtained and the arrangement of different types of cuticle was demonstrated. The membrane connects all structures of the system and divides the terminal parts of the claw flexor muscle into the external (unguitractor plate) (UT) and inner (tendon) ones. Elastic nonlayered cuticle located between the claws and the posterior wall of the terminal tarsomere is interpreted as a claw-returning string. Cuticle surrounding the apodeme of the posterior wall of the terminal tarsomere contains large porous canals. The anterior part of the terminal tarsomere has an invagination that forms a plate facing toward the UT. This plate comprises the UT anteriorly and laterally and contains a microtrichia field (MF) on its distal part. The surface of the UT has a complex microstructure providing fixation to the MF of the corresponding surface of the anterior wall of the terminal tarsomere. Microtrichia of the UT and MF are directed to opposite directions and provide anchorage of the UT whenever the flexor claw muscle contracts. The microsculpture of UT and MF for representatives of Odonata, Coleoptera, Hemiptera, Hymenoptera, and Diptera was compared. It is suggested that small insects, which are able to walk quickly on thin rods, usually have wide microplates on the UT plate to provide quicker fixation-release of the UT in the contact area. Insects using the legs to produce hollows in the soil usually have a large UT with well-developed microtrichia on its surface to produce strong friction forces in the contact area for a long period of time. © 1996 Wiley-Liss, Inc.     

Reaction of parasitoids of the paper wasp Polistes dominulus (Christ) (Hymenoptera, Vespidae, Polistinae) to the host distribution

The specific features of spatio-temporal organization of the parasitoid-host system in a heterogeneous environment was analyzed. The spatial distribution of ectoparasitoids in different habitat types of their host Polistes dominulus (Christ) (Hymenoptera, Vespidae) was found to be non-uniform. Latibulus argiolus (Rossi) (Hymenoptera, Ichneumonidae) prevailed in the host nests located in shelters, while Elasmus schmitti Ruschka (Hymenoptera, Eulophidae) prevailed in the nests attached to plants.     

Pretarsus and distal margin of the terminal tarsomere as an unexplored character system for higher‐level classification in Cholevinae (Coleoptera,Leiodidae)

Cholevinae are well founded as a monophylum, but their internal phylogenetic relationships constitute a matter of longstanding dispute. The morphology has been the main source of information in most available phylogenetic studies on the subfamily. Most of the characters used, however, were limited to easily visible external structures and genitalia. Here we investigate the informative power of an unexplored character system for the higher‐level systematics of Cholevinae: the morphology of the pretarsus and distal margin of the terminal tarsomere. We analysed and documented these structures in representatives of the five most species‐rich tribes of Cholevinae (encompassing 13 subtribes) using scanning electron microscopy. We identified several diagnostic features and recognize potential synapomorphies at the tribal, subtribal and generic levels. The architecture of the median and empodial sclerites (including the empodial setae), the shape and composition of the medial projection of the distal margin of the terminal tarsomere, and the armature of the claws were considered a promising source of information for delimiting tribes and subtribes. Our data challenge the traditional view of a close proximity of Eucatopini and Ptomaphagini as well as a previously suggested synapomorphy of Leptodirini, and reinforce the monophyly of Ptomaphagini. This contribution is one of the rare comparative studies on the coleopteran pretarsus and one of very few evaluating the systematic usefulness of the distal margin of the terminal tarsomere in insects.     

Marked sperm dimorphism in the ground beetle Scarites terricola: a novel type of insect sperm polymorphism

Sperm polymorphism describes the phenomenon of male ejaculates containing two or more distinct types of sperm. In insects, four types of sperm polymorphism are recognized in species from the orders Diptera, Hemiptera, Hymenoptera, Lepidoptera and Coleoptera. The present study describes dimorphic sperm of the ground beetle Scarites terricola (Coleoptera: Carabidae) as a novel type of sperm polymorphism in insects. Sperm from the spermatophore and male seminal vesicles are examined at the light‐microscopic level, and both display marked dimorphism. One type has sperm formed into bundles, in which the head of numerous spermatozoa are ‘glued’ together, with tails free‐moving. The other type are free as single spermatozoa and have a disproportionately large‐sized head and an elongated tail. Both types are motile in Ringer's solution. The adaptive and phylogenetic importance of these findings is discussed.     

On the edge of parasitoidism: a new Lower Cretaceous woodwasp forming the putative sister group of Xiphydriidae + Euhymenoptera

The fossil woodwasp Cratoenigma articulata gen. et sp.n. (Insecta: Hymenoptera) is described from the Lower Cretaceous Crato formation of Brazil. This fossil cannot be placed in any existing superfamily, but its putative phylogenetic position within Hymenoptera is discussed in detail on the basis of relevant thoracic, abdominal and wing venation characters. These characters are critically evaluated and compared with those of extant and fossil Hymenoptera. The phylogenetic position of C. articulata sp.n. is investigated relative to extant Xyelidae, Tenthredinoidea s.l., Pamphilioidea, Cephidae, Siricoidea, Xiphydriidae, Orussidae and Apocrita, and also to Mesozoic Gigasiricidae, Myrmiciidae, Daohugoidae, Sepulcidae, Anaxyelidae, Paroryssidae and Ephialtitidae. Based on the presence of a synapomorphic transscutal articulation, a plesiomorphic unconcealed mesopostnotum and autapomorphic hindwing venation (cu‐a distinctly basal to fork between M and Cu), C. articulata sp.n. most likely forms the sister group of Xiphydriidae + Euhymenoptera. This would place it well within Unicalcarida, i.e. the clade in which the transition from endophytic to parasitoid lifestyle evolved.     

Evolution of locomotory attachment pads in the Dermaptera (Insecta)

This contribution is the first comparative SEM study of tarsal and pretarsal structures of 18 dermapteran species, including epizoic Hemimeridae, rare Apachyidae, as well as basal Pygidicranidae. Our data reject the apparent uniformity of this taxon and show that representatives of Dermaptera have independently evolved both types of attachment mechanisms: hairy and smooth. Dermaptera possess a wide spectrum of attachment devices: arolia, euplantulae, tarsal surfaces covered with specialised tenent setae and other types of cuticular outgrowths. The groundpattern of the pretarsal and tarsal attachment structures was reconstructed by mapping their characters onto a cladogram, generated without tarsal characters. In the groundpattern of recent Dermaptera, the tarsus consists of three tarsomeres. Presumably, the last common ancestor of the Dermaptera possessed an arolium, since this structure occurs in the most basal taxa: Diplatyidae, Karschiellidae (partim, adults), Pygidicranidae partim, and Apachyidae. The absence of arolium in two of the pygidicranid taxa is probably due to a secondary loss. The arolium seems to be reduced in the 'higher Dermaptera' and amongst them, only the Geracinae, which belong to the Spongiphoridae and, hence, to the well supported Eudermaptera [European Journal of Entomology, 98 (2001), 445], evolved this structure convergently. The character state distribution for euplantulae suggests their evolution being similar to that of the arolium. All species of Tagalina possess a specialised tarsus with a strongly dilated second tarsomere. The same applies to the Forficulidae. However, their relatively remote phylogenetic position to Tagalina burri is a convincing reason to assume convergent evolution of this character. The Chelisochidae, with a slender, elongated second tarsomere, possess a unique structure, which supports their monophyly. The special, heart shaped structure of the second tarsal segments in the Forficulidae suggests their monophyly. The attachment structures of Hemimerus vosseleri are highly derived and probably autapomorphic for this taxon.     

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.     

The problem of the number of tarsomeres in the regenerated cockroach leg.

There are 5 tarsomeres in the normal cockroach leg, but this number is often reduced in regenerated legs. In order to examine this complicated situation, fore-, mid-, and hindlegs of German cockroaches were amputated at 11 different tarsal levels and at 18 different times during the last instar. When tarsi were amputated at or proximal to the 3rd tarsomere, 4-segmented tarsi regenerated. When legs were amputated distal to the 3rd tarsomere, the regenerated tarsi had 5 segments. Three-segmented tarsi rarely regenerated when legs were amputated proximal to 3rd tarsomere and in the latter half of the instar period. The lengths of all tarsomeres of regenerated tarsi were measured together with those of unoperated contralateral tarsomeres, and the ratios of the former to the latter were calculated. The ratios ranged from 28 to 138% for the various tarsomeres and levels of amputation. From a comparison of the ratios and morphological observations, it was suggested that the 3rd tarsomere of the normal 5-segmented tarsus has disappeared in the regenerated 4-segmented tarsus. Pads and disto-lateral spines of tarsomeres were observed on unoperated and regenerated tarsi. It was of interest that double spines were often found on the 4-segmented tarsi, mostly on the 2nd tarsomere, just proximal to the position of the missing 3rd tarsomere. This observation supported the idea that the 3rd tarsomere has not simply disappeared, but has probably fused with the 2nd tarsomere.     

Description of the antennal sensilla of <Emphasis Type="Italic">Habrobracon Hebetor</Emphasis>

The morphology of the antennal sensilla of both male and female Habrobracon hebetor (Say) (Hymenoptera: Braconidae) is described using Scanning Electron Microscopy complemented with Transmission Electron Microscopy. Five types of innervated sensilla as well as uninnervated microtrichia were found. These types are: sensilla trichodea; s. chaetica; s. basiconica; s. coeloconica; and s. placodea. No differences in shape, basic structure, and types of antennal sensilla were found between males and females. The types of sensilla of both sexes of H. hebetor were compared with what has been described in other parasitic Hymenoptera, and their putative functions are discussed with reference to their morphology, distribution and ultrastructure.     

Morphological and electrophysiological mapping of tarsal chemoreceptors of oviposition-deterring pheromone in Rhagoletis pomonella flies

Light microscopy and S.E.M. observations revealed that Rhagoletis pomonella female tarsi, bearing the principal receptors of oviposition-deterring fruit marking pheromone (ODP), have 3 types of chemosensilla: B, C and D. Using electrophysiological hair tip-recording techniques, we found that D chemosensilla located in pairs on distal ventrolateral portions of the 2nd, 3rd and 4th tarsomeres of each leg were highly sensitive to stimulation by the pheromone. D chemosensilla located in pairs on the 5th tarsomere of each leg were moderately sensitive to the pheromone, while the B and C chemosensilla of all tarsi were nearly or completely insensitive to it. For reasons discussed, the D chemosensilla on the prothoracic tarsi may be the most important in providing sensory input eliciting oviposition deterrence.     

How do insect nuclear ribosomal genes compare to protein-coding genes in phylogenetic utility and nucleotide substitution patterns?

Abstract. The expanding data set on insect molecular systematics allows examination of phylogenetic performance and molecular evolution of different types of gene. Studies combining more than one gene in the same analysis allow examination of the relative contribution and performance of each gene partition and can help inform gene choice for resolving deep and/or problematic divergences. We compared results obtained from analyses of twelve insect data sets in which authors combined one or more nuclear ribosomal genes (28S and/or 18S) with one or more protein-coding genes [elongation factor-1α (EF-1α), histone H3, carbamoylphosphate synthetase domain (CPS domain of CAD, or rudimentary), long-wavelength rhodopsin (LW opsin), glucose-6-phosphate dehydrogenase (G₆pd), phosphoenolpyruvate carboxykinase (PEPCK), arginine kinase, and white]. Data sets examined spanned eight orders of insects (Odonata, Ephemeroptera, Hemiptera, Coleoptera, Trichoptera, Lepidoptera, Diptera and Hymenoptera), providing a broad range of divergence times and taxonomic levels. We estimated the phylogenetic utility of the individual genes (using parsimony methods) and characterized the nucleotide substitution patterns (using Bayesian methods) to ask which type of data is preferable for phylogenetic analysis in insects. Nuclear ribosomal and protein coding genes differed little in our measures of phylogenetic performance and patterns of nucleotide substitution. We recommend combining nuclear ribosomal gene data with nuclear protein-coding gene data because each data set has distinct advantages. We do not recommend using mitochondrial genes for higher-level studies of insect phylogeny because reviewed studies demonstrate substitution patterns that lead to high levels of homoplasy.     

Review of morphological evidence on the phylogeny of basal Hymenoptera (Insecta), with a discussion of the ordering of characters

In a previous study of the phylogeny of basal Hymenoptera, Vilhelmsen (2001; Zool. J. Linn. Soc . 131 : 393–442) compiled an extensive morphological data matrix for a phylogenetic analysis of basal Hymenoptera, comprising 38 hymenopteran genera. In this study, his characters are revised. This results in a cladogram whose relationships largely agree with those proposed by Vilhelmsen, except that the relationships at the base of the Hymenoptera are unresolved. The revised data matrix is expanded by 17 sawfly and three apocritan taxa. Moreover, 112 new morphological characters from different parts of the larval and adult morphology are also added to the data matrix, including 82 from a recent study of the terminal abdominal segments of male Hymenoptera. The addition of the new characters leads to Xyelidae, again, being the sister-group of all other Hymenoptera. The relationships among the sawfly families as proposed by Vilhelmsen are confirmed, except that the relationships among Syntexis , Siricidae and Xiphydriidae + Vespina are unresolved and that the monophyly of Apocrita is not convincingly supported. A separate analysis is performed which includes all extant genera of Xyelidae. The internal phylogeny of Xyelidae is determined as (( Macroxyela Megaxyela ) Xyelecia ( Xyela Pleroneura )).  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 209–243.     

Gross morphology of multiporous plate sensilla in the Hymenoptera (Insecta)

Both external and internal gross morphology of multiporous plate sensilla were investigated throughout the Hymenoptera, with particular reference to nonaculeate families, using SEM. Several scenarios concerning the origin of multiporous plate sensilla are discussed. Shape, attachment, position, and reinforcing structures, were found to vary between the families, and the possible phylogenetic implications of these are discussed.     

Near intron positions are reliable phylogenetic markers: an application to holometabolous insects

Today, the reconstruction of the organismal evolutionary tree is based mainly on molecular sequence data. However, sequence data are sometimes insufficient to reliably resolve in particular deep branches. Thus, it is highly desirable to find novel, more reliable types of phylogenetic markers that can be derived from the wealth of genomic data. Here, we consider the gain of introns close to older preexisting ones. Because correct splicing is impeded by very small exons, nearby pairs of introns very rarely coexist, that is, the gain of the new intron is nearly always associated with the loss of the old intron. Both events may even be directly connected as in cases of intron migration. Therefore, it should be possible to identify one of the introns as ancient (plesiomorphic) and the other as novel (derived or apomorphic). To test the suitability of such near intron pairs (NIPs) as a marker class for phylogenetic analysis, we undertook an analysis of the evolutionary positions of bees and wasps (Hymenoptera) and beetles (Coleoptera) in relation to moths (Lepidoptera) and dipterans (Diptera) using recently completed genome project data. By scanning 758 putatively orthologous gene structures of Apis mellifera (Hymenoptera) and Tribolium castaneum (Coleoptera), we identified 189 pairs of introns, one from each species, which are located less than 50 nt from each other. A comparison with genes from 5 other holometabolan and 9 metazoan outgroup genomes resulted in 22 shared derived intron positions found in beetle as well as in butterflies and/or dipterans. This strongly supports a basal position of hymenopterans in the holometabolous insect tree. In addition, we found 31 and 12 intron positions apomorphic for A. mellifera and T. castaneum, respectively, which seem to represent changes inside these branches. Another 12 intron pairs indicate parallel intron gains or extraordinarily small exons. In conclusion, we show here that the analysis of phylogenetically nested, nearby intron pairs is suitable to identify evolutionarily younger intron positions and to determine their relative age, which should be of equal importance for the understanding of intron evolution and the reconstruction of the eukaryotic tree.     

Mitochondrial DNA diversity and geographical distribution of sexual and asexual strains of the braconid parasitoid Meteorus pulchricornis

Asexuality is an important tool with regard to the use of parasitoid wasps as biocontrol agents. Asexual (apomictic thelytokous) strains of Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae), a polyphagous endoparasitoid of lepidopteran larvae, are sympatric with sexual (arrhenotokous) strains in Japan. The results of phylogenetic analyses of mitochondrial cytochrome c oxidase subunit I (COI) sequences indicated two major haplotype groups on the Japanese islands. The northern group I predominantly contained sexual strains, whereas the southern group II contained both sexual and asexual strains. Most asexual strains were likely derived within group II. An asexual strain recently established in New Zealand has the identical haplotype to a strain in Japan and was proven to have originated from East Asia. Three hypotheses on the evolution of asexuality are discussed for this parasitoid wasp: recessive gene, hybridization, and cytoplasmic element.     

Grooming behaviours in the Hymenoptera (Insecta): potential phylogenetic significance

Grooming behaviours from representatives of 36 families of Hymenoptera were video recorded and analysed. Thirty-three distinct types of grooming movements were recognized. The evolutionary pattern of each behaviour is discussed. Some behaviours displayed consistent variation between taxa, and appear to be informative regarding higher level relationships within the order. Putative synapomorphies are reported that support the monophyly of the Apocrita, Cynipoidea, Platygastroidea, Ichneumonoidea, and Chalcidoidea including the Mymaridae.     

Giant stick insects reveal unique ontogenetic changes in biological attachment devices

A strong modification of tarsal and pretarsal attachment pads during the postembryonic development is described for the first time. In the exceptionally large thorny devil stick insect Eurycantha calcarata a functional arolium is only present in the immature instars, enabling them to climb on smooth surfaces, especially leaves. Nymphs are also characterized by greyish and hairy euplantulae on tarsomeres 1–4. The gradual modifications of the arolium and the euplantula of tarsomere 5 in the nymphal development are probably mainly related to increased weight. The distinct switch in the life style between the leaf-dwelling nymphal stages and the ground-dwelling adults results in the final abrupt change of the adhesive devices, resulting in a far-reaching reduction of the arolium, the presence of a fully-developed, elongated euplantula on tarsomere 5, and white and smooth euplantulae on tarsomeres 1–4. The developmental remodelling of attachment pads also reflects a phylogenetic pattern. The attachment devices of the earlier instars are similar to those found in the basalmost lineage of extant stick insects, Timema, which is characterized by a very large pan-shaped arolium and a hairy surface of the tarsal and pretarsal attachment pads.     

Staminodes: Their morphological and evolutionary significance

Different approaches to circumscribe staminodial structures in the angiosperms are reviewed. The need for a morphological distinction between “true staminodes” (derived from stamens or homologous to stamens) and “pseudostaminodes” (nonhomologous to stamens) is emphasized. In phylogenetic studies the term “staminode” is often used uncritically, without knowledge of the true homology of these structures. Staminodes are either whole organs (outer tiers or whorls, namely petals, intermediate tiers, or organs within a tier), or partial organs. This article aims to discuss the shortcomings of the past and current approach of staminodes and proposes definitions of staminode types for use as characters in phylogenetic analyses. Staminodial structures should be classified according to their position and function in the flower. Both aspects are intricately linked and make the identification of staminodes sometimes problematic. Shifts in time (heterochrony) and space (heterotopy or homeosis) make that a regressing organ either aborts completely or becomes remodeled into something new. Petals are included in the definition of staminodes as they combine function and heterotopy. A hierarchical ordering of staminodial types is given and discussed. Three interdependent but possibly complementary functions are attached to the occurrence of staminodes: an attractive, nutritional, and structural function. The importance of staminodes for the evolution of the androecium and flower is demonstrated. The difficulty in unmasking pseudostaminodes, comprising receptacular disks, is demonstrated. The value and shortcomings of molecular-based interpretations of staminodes are discussed. It is shown that the decision to recognize a staminode from receptacular emergences often relies on unstable grounds and remains largely dependent on the acceptance of a given phylogenetic background.