Christiane Weirauch

Systematics and Evolution of Heteroptera: 25 Years of Progress

Heteroptera, or true bugs, are part of the most successful radiation of nonholometabolous insects. Twenty-five years after the first review on the influence of cladistics on systematic research in Heteroptera, we summarize progress, problems, and future directions in the field. The few hypotheses on infraordinal relationships conflict on crucial points. Understanding relationships within Gerromorpha, Nepomorpha, Leptopodomorpha, Cimicomorpha, and Pentatomomorpha is improving, but progress within Enicocephalomorpha and Dipsocoromorpha is lagging behind. Nonetheless, the classifications of several superfamily-level taxa within the Pentatomomorpha, such as Aradoidea, Coreoidea, and Pyrrhocoroidea, are still unaffected by cladistic studies. Progress in comparative morphology is slow and drastically impedes our understanding of the evolution of major clades. Molecular systematics has dramatically contributed to accelerating the generation and testing of hypotheses. Given the fascinating natural history of true bugs and their status as model organisms for evolutionary studies, integration of cladistic analyses in a broader biogeographic and evolutionary context deserves increased attention.

Phylogenetic relationships within the Cimicomorpha (Hemiptera: Heteroptera): a total‐evidence analysis

Abstract A phylogenetic analysis for the Cimicomorpha was conducted using 92 taxa, including eight outgroups and six species of Thaumastocoridae. Density of taxon sampling allows for tests of relationships at the family level for most taxa, whereas in the Miridae denser sampling allows for doing so on the tribal level. This level of sampling also corresponds with the availability of testable published hypotheses of relationships. Morphological data for 73 characters are coded for all taxa. Approximately 3500 base pairs of DNA were sequenced for the following gene regions for 83 taxa: 16S rDNA, 18S rDNA, 28S rDNA and COI. Results are presented for analysis of morphological data, individual molecular partitions, combined molecular data, combined morphological and molecular data for 83 taxa and combined morphological and molecular data for 92 taxa. Analyses of morphological data were performed using the parsimony programs nona and piwe: molecular and combined data were analysed using direct optimization with the program poy. Major conclusions of the present study include recognition of the following monophyletic groups: The Geocorisae is a monophyletic group. The monophyly of the Cimicomorpha – including Thaumastocoridae – is not supported in most analyses. The Reduviidae is monophyletic, with the Phymatinae Complex being the sister‐group of the remaining subfamilies. The circumscription of the Cimiciformes is altered from the prior conception of Schuh and Štys to also include the Joppeicidae, Microphysidae and Velocipedidae, as well as the recently described family Curaliidae; the monophyly of the Cimiciformes is supported in most analyses; the Cimiciformes is treated as the sister‐group of the Miroidea in most analyses. The monophyly of the Cimicoidea, including Curaliidae, is supported in all analyses including molecular data, whereas Curaliidae is treated as a more basal cimiciform in all other analyses. The monophyly and placement of the Thaumastocoridae is ambiguous across the range of analyses, and the monophyly of the Miroidea sensu Schuh and Štys receives limited support in the combined analyses of morphology + molecular data. The Tingidae and Miridae are each monophyletic and together almost invariably form a monophyletic group. Within the Miridae, several inclusive monophyletic groups at the subfamily/tribal level are more or less consistently recognized when molecular data are included; however, the interrelationships of the subfamilies vary substantially across the range of analyses. Of the individual molecular partitions, only 18S rDNA shows significant congruence with combined analyses of morphological, combined molecular or combined morphological and molecular data. Scenarios are discussed for the evolution of the metathoracic scent‐efferent system and the origin of the fossula spongiosa.

Cladistic analysis of Reduviidae (Heteroptera: Cimicomorpha) based on morphological characters

Abstract With more than 6600 species worldwide, Reduviidae (Insecta: Heteroptera), or assassin bugs, form the second largest and one of the most diverse groups of true bugs. The poor condition of the higher‐level classification of Reduviidae is reflected by the facts that different authors recognize between 21 and 32 subfamily‐level names and that Reduviidae were never subjected to a rigorous cladistic analysis using an exemplar approach. In the present study, a cladistic analysis of higher‐level taxa of Reduviidae based on 162 morphological characters and 75 ingroup and outgroup species is presented. Twenty‐one subfamily‐level taxa of Reduviidae were examined, accounting for 28 tribes. In addition to characters previously used for diagnosis in Reduviidae, information on recently published character complexes is used in the present analysis, supplemented with new character information gathered specifically for this project. Reduviidae are supported as a monophyletic group with Pachynomidae as their sister taxon. The major results of this study are the support of a sistergroup relationship of Hammacerinae with the remaining Reduviidae, the monophyly of the Phymatine Complex, the relatively basal position of Harpactorinae within Reduviidae as well as a novel hypothesis on the relationships within this group, and the sistergroup relationship of Ectrichodiinae + Tribelocephalinae and their placement in a clade that also contains Emesinae, Saicinae, and Visayanocorinae. The analysis further supports a clade formed by paraphyletic Salyavatinae + Sphaeridopinae, renders Vesciinae non‐monophyletic, and demonstrates the polyphyly of Reduviinae. Pseudocetherinae are shown to group with some Reduviinae. Triatominae are supported as a monophyletic group and are nested among additional Reduviinae and Stenopodainae.

Evolutionary History of Assassin Bugs (Insecta: Hemiptera: Reduviidae): Insights from Divergence Dating and Ancestral State Reconstruction

Assassin bugs are one of the most successful clades of predatory animals based on their species numbers (∼6,800 spp.) and wide distribution in terrestrial ecosystems. Various novel prey capture strategies and remarkable prey specializations contribute to their appeal as a model to study evolutionary pathways involved in predation. Here, we reconstruct the most comprehensive reduviid phylogeny (178 taxa, 18 subfamilies) to date based on molecular data (5 markers). This phylogeny tests current hypotheses on reduviid relationships emphasizing the polyphyletic Reduviinae and the blood-feeding, disease-vectoring Triatominae, and allows us, for the first time in assassin bugs, to reconstruct ancestral states of prey associations and microhabitats. Using a fossil-calibrated molecular tree, we estimated divergence times for key events in the evolutionary history of Reduviidae. Our results indicate that the polyphyletic Reduviinae fall into 11–14 separate clades. Triatominae are paraphyletic with respect to the reduviine genus Opisthacidius in the maximum likelihood analyses; this result is in contrast to prior hypotheses that found Triatominae to be monophyletic or polyphyletic and may be due to the more comprehensive taxon and character sampling in this study. The evolution of blood-feeding may thus have occurred once or twice independently among predatory assassin bugs. All prey specialists evolved from generalist ancestors, with multiple evolutionary origins of termite and ant specializations. A bark-associated life style on tree trunks is ancestral for most of the lineages of Higher Reduviidae; living on foliage has evolved at least six times independently. Reduviidae originated in the Middle Jurassic (178 Ma), but significant lineage diversification only began in the Late Cretaceous (97 Ma). The integration of molecular phylogenetics with fossil and life history data as presented in this paper provides insights into the evolutionary history of reduviids and clears the way for in-depth evolutionary hypothesis testing in one of the most speciose clades of predators.

Molecular phylogeny of the assassin bugs (Hemiptera: Reduviidae), based on mitochondrial and nuclear ribosomal genes.

The first comprehensive cladistic analysis of Reduviidae, the assassin bugs, based on molecular data is presented and discussed in the context of a recently-published morphological analysis. Assassin bugs are essential components of ecosystems, but also important in agriculture and medicine. Sampling included 94 taxa (89 Reduviidae, 5 outgroups) in 15 subfamilies and 24 tribes of Reduviidae and is based on approximately 3300 base pairs of mitochondrial (16S) and nuclear (18S, 28SD2, 28SD3-5) ribosomal DNA. Partitions of the dataset were aligned using different algorithms implemented in MAFFT and the combined dataset was analyzed using parsimony, partitioned maximum likelihood and partitioned Bayesian criteria. Clades recovered in all analyses, independent of alignment and analytical method, comprise: Cimicomorpha and Reduviidae; Hammacerinae; Harpactorinae; Apiomerini; Peiratinae; Phymatinae; Salyavatinae; Triatominae; Phymatinae+Holoptilinae; the higher Reduviidae (Reduviidae excluding Hammacerinae and the Phymatine Complex); Ectrichodiinae+Tribelocephalinae; (Triatominae+Zelurus)+Stenopodainae. Hammacerinae are rejected as sister group to all remaining Reduviidae in all analyses, as is the monophyly of Reduviinae, Emesinae and Harpactorini. High support values for Triatominae imply that blood-feeding has evolved only once within Reduviidae. Stenopodainae and part of Reduviinae are discussed as close relatives to Triatominae.

Myrtaceae-Feeding Phylinae (Hemiptera: Miridae) from Australia: Description and Analysis of Phylogenetic and Host Relationships for a Monophyletic Assemblage of Three New Genera

Abstract Three new genera and 25 new species of Myrtaceae-feeding Phylinae are described from Australia. A cladistic analysis of a broader cross section of Australian Phylinae indicates that these taxa all belong to a monophyletic group, on the basis of pretarsal and male genitalic structures. Line drawings are used to present information of male and female genitalic structures; scanning electron micrographs illustrate pretarsal, genitalic, and other morphology. Color digital habitus images are presented for the males and females of all species. Digital images from the field and of pressed specimens are presented for a broad cross section of host plants. The newly described taxa represent a portion of the species of Australian Phylinae known to feed on the Myrtaceae; the remaining Myrtaceae-feeding species belong to other lineages and are therefore excluded from this monograph. Twenty-three of the species are recorded only from southwestern Western Australia; two species are recorded from southeastern South Australia. All species breed on members of the subfamily Myrtoideae, tribes Chamelaucieae and Melaleuceae.

Resin gathering in neotropical resin bugs (Insecta: Hemiptera: Reduviidae): functional and comparative morphology.

Apiomerini (Reduviidae: Harpactorinae) collect plant resins with their forelegs and use these sticky substances for prey capture or maternal care. These behaviors have not been described in detail and morphological structures involved in resin gathering, transfer, and storage remain virtually undocumented. We here describe these behaviors in Apiomerus flaviventris and document the involved structures. To place them in a comparative context, we describe and document leg and abdominal structures in 14 additional species of Apiomerini that represent all but one of the 12 recent genera in the tribe. Based on these morphological data in combination with the behavioral observations on A. flaviventris, we infer behavioral and functional hypotheses for the remaining genera within the tribe Apiomerini. Setal abdominal patches for resin storage are associated with maternal care so far only documented for species of Apiomerus. Based on the occurrence of these patches in several other genera, we propose that maternal care is widespread within the tribe. Ventral abdominal glands are widespread within female Apiomerini. We propose that their products may prevent hardening of stored resins thus providing long‐term supply for egg coating. Judging from the diverse setal types and arrangements on the front legs, we predict six different behavioral patterns of resin gathering within the tribe. J. Morphol., 2011.

Revision and Cladistic Analysis of the Polyozus Group of Australian Phylini (Heteroptera: Miridae: Phylinae)

Abstract Polyozus Eyles and Schuh, 2003 was described as a monotypic genus from New Zealand. Seven new Australian species are described and Orthotylus australianus (Carvalho, 1965) is transferred to Polyozus. Cladistic analysis of the nine species of Polyozus and seven additional, related species resulted in the hypothesis that Polyozus is a monophyletic group, with Ancoraphylus, n.gen., with four species, being its sister group. Another new genus, Exocarpocoris, n.gen., with three species, is the sister group of Ancoraphylus + Polyozus. The three species of Exocarpocoris live on the same host plant, the hemiparasite Exocarpos aphyllus (Santalaceae), and occur sympatrically over most of their distribution. Species of Ancoraphylus and Polyozus are mainly restricted to a variety of legumes, most often Acacia (Fabaceae, Mimosoideae), but also Jacksonia (Fabaceae, Papilionoideae) and Senna (Fabaceae, Caesalpinioideae). Species of Polyozus are widely distributed in Australia. Polyozus galbanus Eyles and Schuh, 2003—originally described from New Zealand—also occurs in New South Wales, South Australia, and Tasmania and is here proposed to have been introduced to New Zealand from Australia along with its host plant.

On the evolution of raptorial legs – an insect example (Hemiptera: Reduviidae: Phymatinae)

The presence of chelate and subchelate fore legs in Phymatinae (Hemiptera: Reduviidae), or ambush bugs, provides a unique opportunity to study the evolution of different types of raptorial legs in a closely related group of arthropods. Themonocorini have simple, possibly raptorial legs, Phymatini and Macrocephalini distinct subchelate fore legs, and the charismatic Carcinocorini are the only insects with a chelate fore leg apart from female dryinid Chysidoidea (Hymenoptera). Relationships between the four phymatine tribes are here analyzed in a cladistic framework thus permitting testable hypotheses on the evolution of raptorial legs. The presented analysis of phymatine tribal level relationships is based on a dataset comprising 11 species of Phymatinae and 54 non‐phymatine Reduviidae and Heteroptera. The molecular data set consists of ∼3500 MAFFT aligned bases of 16S, 28S D2–D3, and 18S ribosomal genes. Parsimony and maximum likelihood analyses resulted in identical topologies for the ingroup with the relationships Themonocorini + (Phymatini + (Carcinocorini + Macrocephalini)) receiving high support values. Eleven morphological characters, eight of them derived from fore leg morphology, were optimized on the parsimony analysis. These optimizations indicate that the ancestral ambush bug had a simple raptorial leg; that size reduction of the tarsus, enlargement of the femur, curvature of the fore tibia, armature of tibia and femur with rows of tiny tubercles that allow for gripping of a prey insect, and the large process on the ventral surface of the femur arose in the common ancestor of Carcinocorini + Macrocephalini + Phymatini. The chelate leg in Carcinocorini is likely derived from a subchelate precursor similar to the one seen in recent Macrocephalini and may have evolved through elongation of the ventral, proximal portion of the fore femur and modification of the median process to form part of the digitus fixus.

Anatomy of Disguise: Camouflaging Structures in Nymphs of Some Reduviidae (Heteroptera)

Abstract Immature stages of Reduvius personatus (Linnaeus) and some other Reduviidae are known to camouflage themselves with a range of materials found in their environment. Even though this behavior has been observed in several species, camouflaging structures have never been studied in a comparative way. This study documents for the first time the structure that is involved in the application of camouflaging material, i.e., the hind tarsal fan, and reveals structures that assure the fastening of the camouflaging material, i.e., anchor setae and trichomes, in eight species representing five subfamilies of Reduviidae. Whereas anchor setae assure the attachment of camouflaging material by their mechanical properties, short-projection trichomes, long-projection trichomes, and grouped trichomes are here proposed to secrete a sticky substance for this purpose. Primary homology hypotheses on the three types of trichomes are proposed. At least in some species, short-projection trichomes appear to be responsible for the fastening of the camouflaging layer close to the integument, whereas long-projection trichomes may hold the outer layer of camouflaging material in place.