The pretarsus in Chalcidoidea (Hymenoptera Parasitica): functional morphology and possible phylogenetic implications

The structure of the pretarsus of chalcid wasps (Hymenoptera: Chalcidoidea) was examined with light and scanning electron microscopy. The pretarsus of these wasps is characterized by a distal elastic widening of the planta that spreads over the arcus, by a pair of folding plates at the dorsal side of the arolium (the dorsal plates), and by the absence of auxiliary sclerites. The surface of the fully spread arolium of chalcids has a spongiform structure. The arcus of chalcids is an apodeme of the planta. The peculiarities of the inverting/everting biomechanics of the pretarsus of chalcids involve: 1) interactions between the elastic part of the planta, the dorsal plates and the manubrium, and 2) the functioning of the elastic part of the planta and the arcus together as a single unit. A single apical seta situated distally from the campaniform sensillae and proximal row of setae on the manubrium are regarded as putative synapomorphies of Chalcidoidea. A manubrium with a distinct proximal row of three setae characterizes almost all Eulophidae, Aphelinidae and Signiphoridae (‘eulophid lineage’) and Tetracampidae, whereas a row of two setae characterizes Mymaridae, Rotoitidae and Trichogrammatidae. Other studied families (Pteromalidae, Eurytomidae, Torymidae, Ormyridae, Eupelmidae, Encyrtidae, Perilampidae), which represent a ‘pteromalid lineage’, are characterized mostly by five setae in a proximal row, which could represent a synapomorphy for these groups, or a symplesiomorphy in Chalcidoidea, depending on rooting. However, the characters may be correlated with differences in body size that characterize the different lineages rather than being phylogenetically important. Other characters that may be phylogenetically informative are: 1) shape of the manubrium (spindle‐like in Mymaridae, Rotoitidae, Trichogrammatidae and the ‘eulophid lineage’, but mostly bottle‐like in representatives of the ‘pteromalid lineage’), and 2) pubescence of the proximal part of the planta (sparse, thick setae in Rotoitidae, Trichogrammatidae and the ‘eulophid lineage’, but dense, slender setae in representatives of the ‘pteromalid lineage’).     

Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach

A phylogeny of the Agaonidae (Chalcidoidea) in their restricted sense, pollinators of Ficus species (Moraceae), is estimated using 4182 nucleotides from six genes, obtained from 101 species representing 19 of the 20 recognized genera, and four outgroups. Data analysed by parsimony and Bayesian inference methods demonstrate that Agaonidae are monophyletic and that the previous classification is not supported. Agaonidae are partitioned into four groups: (i) Tetrapus, (ii) Ceratosolen + Kradibia, (iii) some Blastophaga + Wiebesia species, and (iv) all genera associated with monoecious figs and a few Blastophaga and Wiebesia. The latter group is subdivided into subgroups: (i) Pleistodontes, (ii) Blastophaga psenes and neocaledonian Dolichoris, (iii) some Blastophaga and Wiebesia species, and (iv) Platyscapa, all afrotropical genera and all genera associated with section Conosycea. Eleven genera were recovered as monophyletic, six were para‐ or polyphyletic, and two cannot be tested with our data set. Based on our phylogeny we propose a new classification for the Agaonidae. Two new subfamilies are proposed: Tetrapusiinae for the genus Tetrapus, and Kradibiinae for Ceratosolen + Kradibia. Liporrhopalum is synonymized with Kradibia and the subgenus Valisia of Blastophaga is elevated to generic rank. These changes resulted in 36 new combinations. Finally, we discuss the hypothesis of co‐speciation between the pollinators and their host species by comparing the two phylogenies. © The Willi Hennig Society 2009.     

A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera)

Chalcidoidea (Hymenoptera) is extremely diverse with an estimated 500 000 species. We present the first phylogenetic analysis of the superfamily based on both morphological and molecular data. A web‐based, systematics workbench mx was used to score 945 character states illustrated by 648 figures for 233 morphological characters for a total of 66 645 observations for 300 taxa. The matrix covers 22 chalcidoid families recognized herein and includes 268 genera within 78 of 83 subfamilies. Morphological data were analysed alone and in combination with molecular data from ribosomal 18S (2105 bp) and 28S D2–D5 expansion regions (1812 bp). Analyses were analysed alone and in combined datasets using implied‐weights parsimony and likelihood. Proposed changes in higher classification resulting from the analyses include: (i) recognition of Eriaporidae, revised status; (ii) recognition of Cynipencyrtidae, revised status; (iii) recognition of Azotidae, revised status; (iv) inclusion of Sycophaginae in Agaonidae, revised status; (v) reclassification of Aphelinidae to include Aphelininae, Calesinae, Coccophaginae, Eretmocerinae and Eriaphytinae; (vi) inclusion of Cratominae and Panstenoninae within Pteromalinae (Pteromalidae), new synonymy; (vii) inclusion of Epichrysomallinae in Pteromalidae, revised status. At a higher level, Chalcidoidea was monophyletic, with Mymaridae the sister group of Rotoitidae plus the remaining Chalcidoidea. A eulophid lineage was recovered that included Aphelinidae, Azotidae, Eulophidae, Signiphoridae, Tetracampidae and Trichogrammatidae. Eucharitidae and Perilampidae were monophyletic if Eutrichosomatinae (Pteromalidae) was included, and Eupelmidae was monophyletic if Oodera (Pteromalidae: Cleonyminae) was included. Likelihood recovered a clade of Eupelmidae + (Tanaostigmatidae + (Cynipencyrtus + Encyrtidae). Support for other lineages and their impact on the classification of Chalcidoidea is discussed. Several life‐history traits are mapped onto the new phylogeny.     

Subforaminal bridges in Hymenoptera (Insecta), with a focus on Chalcidoidea

Variation in structures of the posterior surface of the head in Hymenoptera is compared and interpreted according to theories of head capsule evolution, with focus on understanding previously baffling conditions in the superfamily Chalcidoidea. Features are investigated separately without first classifying subforaminal bridges into subcategories. In Proctotrupomorpha (including Chalcidoidea), Ceraphronoidea and some Ichneumonoidea, there are multiple posterior pits associated with the tentorium. In most examined Hymenoptera with a subforaminal bridge, there was a differentiated median area, typically with highly variable microtrichia. This area is elevated in Cephoidea and Pamphilioidea, but is not elevated in other Hymenoptera. Subforaminal bridges in Apocrita previously classified as hypostomal bridges are discussed in the context of A.P. Rasnitsyn's hypothesis that relative importance of adult feeding drives subforaminal bridge evolution.     

Skeletal morphology of Opius dissitus and Biosteres carbonarius (Hymenoptera: Braconidae), with a discussion of terminology

The Braconidae, a family of parasitic wasps, constitute a major taxonomic challenge with an estimated diversity of 40,000 to 120,000 species worldwide, only 18,000 of which have been described to date. The skeletal morphology of braconids is still not adequately understood and the terminology is partly idiosyncratic, despite the fact that anatomical features form the basis for most taxonomic work on the group. To help address this problem, we describe the external skeletal morphology of Opius dissitus Muesebeck 1963 and Biosteres carbonarius Nees 1834, two diverse representatives of one of the least known and most diverse braconid subfamilies, the Opiinae. We review the terminology used to describe skeletal features in the Ichneumonoidea in general and the Opiinae in particular, and identify a list of recommend terms, which are linked to the online Hymenoptera Anatomy Ontology. The morphology of the studied species is illustrated with SEM-micrographs, photos and line drawings. Based on the examined species, we discuss intraspecific and interspecific morphological variation in the Opiinae and point out character complexes that merit further study.     

The larval head morphology of Xyela sp. (Xyelidae, Hymenoptera) and its phylogenetic implications

Larval head structures of Xyela sp. are described in detail. The characters are compared to conditions found in larvae of other groups of Hymenoptera and Endopterygota. Like other symphytan larvae the immature stages of Xyelidae are mainly characterized by presumably plesiomorphic features of the head. The head sutures are well developed and all parts of the tentorium are present. The labrum is free and a complete set of labral muscles is present. The maxillae are in a retracted position. In contrast to other hymenopteran larvae Xyela possesses a clypeofrontal suture, a comparatively long antenna and three well‐developed antennal muscles. Apomorphic features of Xyela are the absence of muscles associated with the salivarium and the complete absence of Musculus craniocardinalis. A clade comprising Orussidae and Apocrita is supported by the unsegmented maxillary and labial palps and the absence of the lacinia. Six potential autapomorphies for the Hymenoptera were revealed: (1) the caudal tentorial apodeme, (2) the bifurcated tendon of Musculus craniomandibularus internus, (3) the lateral lobe of the cardo, (4) the origin of M. tentoriohypopharyngalis from the posterior head capsule, (5) the exceptionally strong prepharyngo‐pharyngeal longitudinal muscle and (6) the longitudinal muscle of the silk press. The maxillolabial complex, the vestigial M. craniocardinalis and a distinctly developed labio‐hypopharyngeal lobe bearing the opening of the salivary duct are potential synapomorphies of Hymenoptera and Mecopterida. The globular, orthognathous head capsule, the modified compound eyes, the occipital furrow and the X‐shaped tentorium are features with unclear polarity shared by Hymenoptera and Mecoptera.     

Cales (Hymenoptera: Chalcidoidea): morphology of an enigmatic taxon with a review of species

Calesinae is a small group of Chalcidoidea (Hymenoptera) that are parasitoids of whiteflies (Hemiptera: Aleyrodidae). One species, Cales noacki Howard, has been introduced from South America into citrus‐growing regions of North America, the Mediterranean and Africa for biological control. The remaining species are found in Australia and New Zealand: a classic Gondwanan disjunction. The subfamily consists of a single genus, Cales, which is currently unplaced within Chalcidoidea. Its taxonomic position has historically been unstable, although most often Cales is associated with Aphelinidae. Here, we present a detailed morphological study of the group with an emphasis on Australian species. Although Cales shares many characteristics with Aphelinidae, especially Coccophaginae and Eretmocerus, more studies of character systems across Chalcidoidea are needed to determine which features may be synapomorphic. Consequently, we leave Cales incertae sedis within Chalcidoidea. We also describe a new species from New Zealand, Cales berryi sp.n. , reared from the whitefly Asterochiton pittospori on lemonwood, Pittosporum eugenioides, and we present a key and review the four known species of Cales.     

Cranial morphology of Ateleopus japonicus (Ateleopodidae: Ateleopodiformes), with a discussion on metamorphic mouth migration and lampridiform affinities

The cranial osteology and myology in the ateleopodiform Ateleopus japonicus were studied. Many free bony ossicles constitute the cephalic lateral line canals and are separated from the neurocranial roof by thick gelatinous tissue. The preoperculomandibular canal is unique in having a direct connection with the infraorbital canal owing to strong reduction in the size of the preoperculum. The neurocranium is largely cartilaginous, with 6 chondrocranial and 1 dermal element being absent (or not undergoing ossification). The left and right frontals are separated by a deep groove into which a long, mobile rostral cartilage is deeply inserted. Five pairs of cartilages, including 2 pairs of menisci, are associated with the ethmoid region, allowing premaxillary protrusion without involving maxillary rotation. The levator operculi is well developed and likely generates the primary force for depressing the lower jaw. The large interhyal is tightly attached to the entire ventral margin of the operculum, and the two elements appear to function as a single unit in mouth opening. The oral cavity is large because of the posterior position of the branchial arches [the last (5th) arch is situated below the 3rd vertebra]. In pelagic individuals the head is flat with a terminal mouth and straight parasphenoid shaft, whereas in small, benthopelagic individuals the head is rounded with an inferior mouth and bent parasphenoid shaft. “Bending” of the parasphenoid with a dorsally elevated apex is considered the result of the posterior migration of the mouth during the habitat shift. Ateleopodiform characters are discussed phylogenetically and the deep insertion of the rostral cartilage into an open space in the ethmoid region is suggested as a synapomorphy of the order and Lampridiformes.     

Ultra‐Conserved Elements and morphology reciprocally illuminate conflicting phylogenetic hypotheses in Chalcididae (Hymenoptera,Chalcidoidea)

Recent technical advances combined with novel computational approaches have promised the acceleration of our understanding of the tree of life. However, when it comes to hyperdiverse and poorly known groups of invertebrates, studies are still scarce. As published phylogenies will be rarely challenged by future taxonomists, careful attention must be paid to potential analytical bias. We present the first molecular phylogenetic hypothesis for the family Chalcididae, a group of parasitoid wasps, with a representative sampling (144 ingroups and seven outgroups) that covers all described subfamilies and tribes, and 82% of the known genera. Analyses of 538 Ultra‐Conserved Elements (UCEs) with supermatrix (RAx ML and IQTREE) and gene tree reconciliation approaches (ASTRAL, ASTRID) resulted in highly supported topologies in overall agreement with morphology but reveal conflicting topologies for some of the deepest nodes. To resolve these conflicts, we explored the phylogenetic tree space with clustering and gene genealogy interrogation methods, analyzed marker and taxon properties that could bias inferences and performed a thorough morphological analysis (130 characters encoded for 40 taxa representative of the diversity). This joint analysis reveals that UCEs enable attainment of resolution between ancestry and convergent/divergent evolution when morphology is not informative enough, but also shows that a systematic exploration of bias with different analytical methods and a careful analysis of morphological features is required to prevent publication of artifactual results. We highlight a GC content bias for maximum‐likelihood approaches, an artifactual mid‐point rooting of the ASTRAL tree and a deleterious effect of high percentage of missing data (>85% missing UCEs) on gene tree reconciliation methods. Based on the results we propose a new classification of the family into eight subfamilies and ten tribes that lay the foundation for future studies on the evolutionary history of Chalcididae.     

Phylogenetic implications of the mesofurca in Chalcidoidea (Hymenoptera), with emphasis on Aphelinidae

The skeletomusculature of the mesofurcal–mesopostnotal complex is surveyed within the Chalcidoidea. Four internal character systems are assessed for their phylogenetic significance: the mesofurcal bridge, the structure and position of the furcal–laterophragmal muscle, the structure of the lateral arms of the mesofurca, and the supporting structures for the interfurcal muscles. Among Hymenoptera, Chalcidoidea are unique in having the furcal–laterophragmal muscle attached along the entire length of the laterophragmal apodeme. Also the furcal–laterophragmal muscle originates medial to the junction of the mesofurcal bridge and lateral mesofurcal arm in most Chalcidoidea. Mymarommatidae do not share either of these apomorphic states with Chalcidoidea. Within Chalcidoidea, apomorphic character states were found in each of Aphelinidae, Encyrtidae, Eulophidae, Mymaridae, Rotoitidae, Signiphoridae, Tanaostigmatidae and Trichogrammatidae. For taxa classified as Aphelinidae, the plesiomorphic complement of structures and muscle attachments is retained in Eriaphytinae and Eriaporinae. The mesofurcal bridge is considered to have been lost at least twice in each of Aphelininae and Coccophaginae. Similar interfurcal processes, resulting from loss of the mesofurcal bridge, support the monophyly of Aphelininae (Aphelinini, Aphytini and Eutrichosomellini). Azotinae are placed as the sister group of Aphelininae because of a similar lateral origin of the laterophragmal muscle and the shape of the mesofurcal arms. Other than loss of the mesofurcal bridge, no character states were shared by Azotinae and Coccophaginae. Coccophaginae (Coccophagini and Pteroptricini) are regarded as monophyletic based on the loss of the mesofurcal bridge, the peculiar shape of the mesofurca, and a unique modification of the laterophragmal muscle. Euxanthellus is removed from synonomy with Coccophagus and may be best treated as a separate tribe of Coccophaginae based on the shape of the lateral mesofurcal arms and the presence of a mesofurcal bridge. The shape of the mesofurca suggests a monophyletic grouping of Cales, Eretmocerus and Trichogrammatidae that could render Aphelinidae paraphyletic.     

Combined molecular and morphological phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with focus on the subfamily Entedoninae

A new combined molecular and morphological phylogeny of the Eulophidae is presented with special reference to the subfamily Entedoninae. We examined 28S D2–D5 and CO1 gene regions with parsimony and partitioned Bayesian analyses, and examined the impact of a small set of historically recognized morphological characters on combined analyses. Eulophidae was strongly supported as monophyletic only after exclusion of the enigmatic genus Trisecodes. The subfamilies Eulophinae, Entiinae (=Euderinae) and Tetrastichinae were consistently supported as monophyletic, but Entedoninae was monophyletic only in combined analyses. Six contiguous bases in the 3e′ subregion of the 28S D2 rDNA contributed to placement of nominal subgenus of Closterocerus outside Entedoninae. In all cases, Euderomphalini was excluded from Entiinae, and we suggest that it be retained in Entedoninae. Opheliminae n. stat. is raised from tribe to subfamily status. Trisecodes is removed from Entedoninae but retained as incertae sedis in Eulophidae until its family placement can be determined new placement . The genera Neochrysocharis stat. rev. and Asecodes stat. rev. are removed from synonymy with Closterocerus because strong molecular differences corroborate their morphological differences. Closterocerus (Achrysocharis) germanicus is transferred to the genus Chrysonotomyia n. comb. based on molecular and morphological characters.     

Phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with a reclassification of Eulophinae and the recognition that Elasmidae are derived eulophids

Eulophidae is a large and biologically varied family of parasitoid wasps, traditionally split into four subfamilies; Elasmidae is a uniform (single genus) and morphologically distinct family of wasps that are thought to be related to Eulophidae. The D2 region of the 28S rDNA gene (≈ 560 bp) of eighty‐seven species of eulophid, three species of elasmid and sixteen outgroup species in five families was sequenced. Cladograms were constructed, and the results compared with conclusions drawn from morphological studies. The gene was most informative at the level of subfamily and tribe. The monophyly of both Eulophinae and Tetrastichinae is supported; that of Entedoninae and Euderinae is less clear. Results indicate that Eulophinae is a derived group within Eulophidae, rather than an ancestral group as previously thought, and that Elasmus, the sole genus of Elasmidae, belongs within this subfamily. The tribes of Eulophinae are reassessed and only three accepted: Eulophini (including Euplectrini and Elachertini), Elasmini and Cirrospilini LaSalle trib.n. for Bou?ek's Ophelimini with Ophelimus and Australsecodes excluded. Three small Australian tribes, Anselmellini, Ophelimini and Platytetracampini, are removed from Eulophinae and Entedoninae, respectively, but their exact relationships and subfamily status cannot as yet be decided. Another tribe, Keryini, known from a single Australian genus, is excluded from both Eulophinae and Eulophidae.     

The ovipositor apparatus of basal Hymenoptera (Insecta): phylogenetic implications and functional morphology

The skeleto‐musculature of the ovipositor apparatus and the external sculpture of the 1st and 2nd valvulae was studied in representatives from all ‘symphytan’ families. Nineteen informative characters were coded and scored. The distribution of character states are discussed with reference to recent cladistic treatments of the Hymenoptera. Putative autapomorphies of the Hymenoptera are the presence of cordate apodemes on T9 and basal articulations and associated musculature between the 2nd valvifers and the 2nd valvulae. It is a ground plan feature of the order to have the gonocoxites of abdominal segment 8 fused with the gonangula. The configuration of the musculature of the ovipositor apparatus did not display much variation among the taxa examined, except within the Pamphilioidea. There is considerable variation in the external ovipositor sculpture within the Tenthredinoidea. Putative synapomorphies for the tenthredinoid families except the Blasticotomidae are the presence of alternating strongly and weakly sclerotized zones on the first and/or second valvulae and the presence of serrulae on the sawteeth. The presence of transverse rows of large ctenidia on the 1st valvulae is an autapomorphy of the Diprionidae. Fusion of the 2nd valvifers and the 3rd valvulae is a synapomorphy for the Argidae + Pergidae. The ovipositor apparatus of the Pamphilioidea is highly derived, putative autapomorphies being the close association between T9 and the first valvifers, the reduction of the distal parts of the 1st valvulae, and the fusion of the 2nd valvulae for their entire length. The changes in the ovipositor apparatus of Pamphilioidea are associated with a decrease in the amount of work it has to perform during ovipositing, as the eggs are placed predominantly externally on the substrate. The ovipositor apparatus of the ‘Siricoidea’ is enlarged and modified for ovipositing into wood. Putative synapomorphies of the ‘Siricoidea’ + Orussidae + Apocrita are the presence of sawteeth only distally on the ovipositor and elongation of the cordate apodemes of T9.     

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.     

Life history and larval morphology of Eurhinus magnificus Gyllenhal (Coleoptera: Curculionidae), a new weevil to the United States

Eurhinus magnificus Gyllenhal has been collected in south Florida, presumably introduced through trade with countries in its native range. Very little information has been published on the biology or taxonomy of this insect. We conducted studies to investigate various aspects of its life history and host plant associations. The pre-imaginal life stages of E. magnificus are described for the first time. Dimensions of the adult, egg, larval, and pupal stages are also provided; head capsule measurement revealed five larval instars. All life stages of E. magnificus were collected at several sites in Broward and Miami-Dade counties from the host plant Cissus verticillata (L.) Nicolson & Jarvis (Vitaceae). Eggs were laid singly within the succulent, young subterminal portion of the host plant stem, one or two occurring between two nodes. Gall formation was apparent by the first to third instar and continued to increase in size until pupation which occurred within the gall. Predators and pathogens appeared to be responsible for considerable mortality in the field; there was no evidence of parasitism of any of the life stages. Greenhouse studies were undertaken to determine E. magnificus development time and host specificity. Adult weevils attacked grape cultivars (Vitis spp.) and feeding opened the stems to fungal agents but no physical evidence of larval development was apparent on grapes.