Revisiting habitat and lifestyle transitions in Heteroptera (Insecta: Hemiptera): insights from a combined morphological and molecular phylogeny

Heteroptera, the true bugs, are part of the largest clade of non-holometabolous insects, the Hemiptera, and include > 42 000 described species in about 90 families. Despite progress in resolving phylogenetic relationships between and within infraorders since the first combined morphological and molecular analysis published in 1993 (29 taxa, 669 bp, 31 morphological characters), recent hypotheses have relied entirely on molecular data. Weakly supported nodes along the backbone of Heteroptera made these published phylogenies unsuitable for investigations into the evolution of habitats and lifestyles across true bugs. Here we present the first combined morphological and molecular analyses of Heteroptera since 1993, using 135 taxa in 60 families, 4018 aligned bp of ribosomal DNA and 81 morphological characters, and various analytical approaches. The sister-group relationship of the predominantly aquatic Nepomorpha with all remaining Heteroptera is supported in all analyses, and a clade formed by Enicocephalomorpha, Dipsocoromorpha and Gerromorpha in some. All analyses recover Leptopodomorpha + (Cimicomorpha + Pentatomomorpha), mostly with high support. Parsimony- and likelihood-based ancestral state reconstructions of habitats and lifestyles on the combined likelihood phylogeny provide new insights into the evolution of true bugs. The results indicate that aquatic and semi-aquatic true bugs invaded these habitats three times independently from terrestrial habitats in contrast to a recent hypothesis. They further suggest that the most recent common ancestor of Heteroptera was predacious, and that the two large predominantly phytophagous clades (Trichophora and Miroidea) are likely to have derived independently from predatory ancestors. We conclude that by combining morphological and molecular data and employing various analytical methods our analyses have converged on a relatively well-supported hypothesis of heteropteran infraordinal relationships that now requires further testing using phylogenomic and more extensive morphological datasets.     

Higher level phylogeny and the first divergence time estimation of Heteroptera (Insecta: Hemiptera) based on multiple genes

Heteroptera, or true bugs, are the largest, morphologically diverse and economically important group of insects with incomplete metamorphosis. However, the phylogenetic relationships within Heteroptera are still in dispute and most of the previous studies were based on morphological characters or with single gene (partial or whole 18S rDNA). Besides, so far, divergence time estimates for Heteroptera totally rely on the fossil record, while no studies have been performed on molecular divergence rates. Here, for the first time, we used maximum parsimony (MP), maximum likelihood (ML) and Bayesian inference (BI) with multiple genes (18S rDNA, 28S rDNA, 16S rDNA and COI) to estimate phylogenetic relationships among the infraorders, and meanwhile, the Penalized Likelihood (r8s) and Bayesian (BEAST) molecular dating methods were employed to estimate divergence time of higher taxa of this suborder. Major results of the present study included: Nepomorpha was placed as the most basal clade in all six trees (MP trees, ML trees and Bayesian trees of nuclear gene data and four-gene combined data, respectively) with full support values. The sister-group relationship of Cimicomorpha and Pentatomomorpha was also strongly supported. Nepomorpha originated in early Triassic and the other six infraorders originated in a very short period of time in middle Triassic. Cimicomorpha and Pentatomomorpha underwent a radiation at family level in Cretaceous, paralleling the proliferation of the flowering plants. Our results indicated that the higher-group radiations within hemimetabolous Heteroptera were simultaneously with those of holometabolous Coleoptera and Diptera which took place in the Triassic. While the aquatic habitat was colonized by Nepomorpha already in the Triassic, the Gerromorpha independently adapted to the semi-aquatic habitat in the Early Jurassic.     

Global diversity of true bugs (Heteroptera; Insecta) in freshwater

The aquatic and semi-aquatic Heteroptera, consisting of the infraorders Leptopodomorpha, Gerromorpha, and Nepomorpha, comprise a significant component of the world’s aquatic insect biota. Within these three infraorders as a whole there are currently 23 families, 343 genera and 4,810 species group taxa considered valid, of which 20 families, 326 genera and 4,656 species inhabit freshwater. In addition, more than 1,100 unequivocally diagnosed species remain to be described. Aquatic Heteroptera occur on all continents except Antarctica, and are most numerous in the tropical regions, although there are many distinctly cold-adapted genera. Overall species richness is highest in the Neotropical and Oriental regions, which harbor 1,289 and 1,103 species, respectively. In comparison to these core tropical regions, species richness is significantly lower in the Afrotropical (799 species), Australasian (654 species), Palearctic (496 species), Nearctic (424 species) and Pacific (37 species) regions. Aquatic Heteroptera are notable for utilizing an exceptionally broad range of habitats, from marine and intertidal to arctic and high alpine, across a global altitudinal range of 0–4,700 m. Species may be found in almost every freshwater biotope, and many exhibit striking morphological adaptations to their aquatic environment, making them excellent subjects for ecological and biogeographic studies. Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

The adipokinetic hormones of Heteroptera: a comparative study

The adipokinetic hormones (AKHs) from 15 species of heteropteran Hemiptera (encompassing eight families, six superfamilies and three infraorders) have been isolated and structurally identified using liquid chromatography coupled with mass spectrometry. None of the structures are novel and all are octapeptides. These peptide sequence data are used, together with the previously available AKH sequence data on Heteroptera, to create a larger dataset for comparative analyses. This results, in total, in AKH sequences from 30 species (spanning 13 families), which are used in a matrix confronted with the current hypotheses on the phylogeny of Heteroptera. The expanded dataset shows that all heteropterans have octapeptide AKHs; three species have two AKHs, whereas the overwhelming majority have only one AKH. From a total of 11 different AKH peptides known from Heteroptera to date, three AKHs occur frequently: Panbo‐red pigment‐concentrating hormone (RPCH) (×10), Schgr‐AKH‐II (×6) and Anaim‐AKH (×4). The heteropteran database also suggests that particular AKH variants are family‐specific. The AKHs of Heteroptera: Pentatomomorpha (all terrestrial) are not present in Nepomorpha (aquatic) and Gerromorpha: Gerridae (semiaquatic); AKHs with a Val in position 2 are absent in the Pentatomomorpha (only AKHs with Leu² are present), whereas Val² predominates in the nonterrestrial species. An unexpected diversity of AKH sequences is found in Nepomorpha, Nepoidea, Nepidae and Nepinae, whereas Panbo‐RPCH (which has been identified in all infraorders of decapod crustaceans) is present in all analysed species of Pentatomidae and also in the only species of Tessaratomidae investigated. The molecular evolution of Heteroptera with respect to other insect groups and to crustaceans is discussed     

Phylogeny of the true water bugs (Nepomorpha: Hemiptera–Heteroptera) based on 16S and 28S rDNA and morphology

Abstract. Morphological characters and molecular sequence data were for the first time analysed separately and combined for the true water bugs (Hemiptera–Heteroptera, infraorder Nepomorpha). Data from forty species representing all families were included, together with two outgroup species representing the infraorders Gerromorpha and Leptopodomorpha. The morphological data matrix consisted of sixty‐five characters obtained from literature sources. Molecular data included approximately 960 bp from the mitochondrial gene 16S and the nuclear gene 28S for all forty‐two terminal taxa. The morphological dataset was analysed using maximum parsimony and the combined morphological and molecular (16S + 28S rDNA) dataset was analysed using direct optimization. A sensitivity analysis of sixteen different sets of parameters (various combinations of insertion–deletion cost and transversion costs) was undertaken. Character congruence was used as an optimality criterion to choose among competing phylogenetic hypotheses. The final hypothesis was obtained from the analysis of the combined molecular and mor phological dataset with the most congruent parameter set. This hypothesis supports the monophyly of all currently recognized families of Nepomorpha, and of the superfamilies Nepoidea (Nepidae + Belostomatidae), Corixoidea (Corixidae), Ochteroidea Ochteridae + Gelastocoridae), Notonectoidea (Notonectidae), and Pleoidea (Pleidae + Helotrephidae), but not the monophyly of the Naucoroidea (Naucoridae + Aphelocheiridae + Potamocoridae). The close relationship between the Notonectidae and Pleoidea is also supported. Our hypothesis concurs with Mahner in the placement of the Corixidae as a sister group to the remaining nepomorphan superfamilies except the Nepoidea, but differs in the placement of the Ochteroidea as a sister group to the Notonectoidea + Pleoidea. The superfamily Naucoroidea should be limited to only including the family Naucoridae and not the families Aphelocheiridae and Potamocoridae. The present analysis strongly supports a sister group relationship between the families Aphelocheiridae and Potamocoridae, a monophylum for which we propose a new superfamily, Aphelocheiroidea.     

Distribution of water bugs (Heteroptera: Nepomorpha, Gerromorpha) over latitudinal zones in the northeast of European Russia

Data on the taxonomic composition of water bugs (Heteroptera: Nepomorpha, Gerromorpha) in the northeast of European Russia are given. A total of 34 water-bug species, which belong to 16 genera and 8 families, are recorded. The species diversity of Nepomorpha and Gerromorpha changes northwards: 33 occur in the taiga zone and only 8 species occur in the tundra zone. The bulk of the fauna consists of Eurosiberian (29%) and trans-Eurasian (26%) species; in latitude-related terms, the temperate group is most richly represented (64%). The species composition of the aquatic and semiaquatic heteropteran fauna of the region is especially similar to that of the tundra and taiga zones of Western Siberia.     

Keys to families and genera of gerromorpha and nepomorpha (Insecta: Heteroptera) in the central Amazonia, Brazil

Few studies have been done in Brazil on aquatic and semi-aquatic Gerromorpha and Nepomorpha (Heteroptera), Minas Gerais being the state where these insects have been studied the most. The present study presents keys for identification of Gerromorpha and Nepomorpha adults, thus providing a tool for ecological studies on aquatic insects in Central Amazonia. The specimens used to elaborate the taxonomic keys were collected in Presidente Figueiredo county in streams and artificial lakes and in Manaus county in streams, white-water floodplain (várzea) lakes and Rio Negro black-water flooded forest (igapó). Specimens from the invertebrate collection of the Instituto Nacional de Pesquisas da Amazonia (INPA) were also examined and included in the keys. Thirty one genera from 13 families of the infra-orders mentioned.     

Phylogenetic analysis of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha): evidence from mitochondrial genomes

Background  

The true water bugs are grouped in infraorder Nepomorpha (Insecta: Hemiptera: Heteroptera) and are of great economic importance. The phylogenetic relationships within Nepomorpha and the taxonomic hierarchies of Pleoidea and Aphelocheiroidea are uncertain. Most of the previous studies were based on morphological characters without algorithmic assessment. In the latest study, the molecular markers employed in phylogenetic analyses were partial sequences of 16S rDNA and 18S rDNA with a total length about 1 kb. Up to now, no mitochondrial genome of the true water bugs has been sequenced, which is one of the largest data sets that could be compared across animal taxa. In this study we analyzed the unresolved problems in Nepomorpha using evidence from mitochondrial genomes.     

The rhabdom structure in the ommatidia of the Heteroptera (Insecta), and its phylogenetic significance

In its plesiomorphic state the insect ommatidium consists of eight retinula cells forming a fused rhabdom. It has long been observed that, in contrast to this pattern, Heteroptera have open rhabdoms. However, there has so far been no comprehensive and comparative study of heteropteran ommatidia. For this reason, we investigated the rhabdom structure in 36 species from all higher groups of Heteroptera, as well as from Coleorrhyncha and Auchenorrhyncha as outgroup representatives. In addition we surveyed the data of earlier authors, which brings the number of examined species to a total of more than 70. All examined Heteroptera do have open rhabdoms, with a system of six peripheral and two central rhabdomeres. Outgroup comparison shows that the open rhabdom is an autapomorphy of the Heteroptera. As for the rhabdom structure within the Heteroptera, we found further autapomorphic patterns in Corixidae (Nepomorpha), Gerromorpha, and Leptopodomorpha. Finally, the Cimicomorpha and Pentatomomorpha share a special pattern of the two central rhabdomeres, which we call V-pattern. This is a new synapomorphy of these two taxa. Accepted: 22 November 1999     

Waterbugs (Heteroptera: Nepomorpha and Gerromorpha) as sources of essential n‐3 polyunsaturated fatty acids in Central Siberian ecoregions

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Phylogeny and diversification of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha)

Climate fluctuations and tectonic reconfigurations associated with environmental changes play large roles in determining patterns of adaptation and diversification, but studies documenting how such drivers have shaped the evolutionary history and diversification dynamics of limnic organisms during the Mesozoic are scarce. Members of the heteropteran infraorder Nepomorpha, or aquatic bugs, are ideal for testing the effects of these determinants on their diversification pulses because most species are confined to aquatic environments during their entire life. The group has a relatively mature taxonomy and is well represented in the fossil record. We investigated the evolution of Nepomorpha based on phylogenetic analyses of morphological and molecular characters sampled from 115 taxa representing all 13 families and approximately 40% of recognized genera. Our results were largely congruent with the phylogenetic relationships inferred from morphology. A divergence dating analysis indicated that Nepomorpha began to diversify in the late Permian (approximately 263 Ma), and diversification analyses suggested that palaeoecological opportunities probably promoted lineage diversification in this group.     

Phylogeny and the colourful history of jewel bugs (Insecta: Hemiptera: Scutelleridae)

Members of the family Scutelleridae (Heteroptera: Pentatomomorpha: Pentatomoidea) are also called shield bugs because of the greatly enlarged scutellum, or jewel bugs because of the brilliant colours of many species. All scutellerids are phytophagous, feeding on various parts of their host plants. Due to lack of obvious synapomorphies and the failure to apply rigorous phylogenetic methods, the higher classification of Scutelleridae has been disputed for more than 150 years. Here we reconstructed a phylogeny of Scutelleridae based on complete sequences of 18S and 28S nuclear rDNAs and all 13 protein‐coding genes of the mitochondrial genome, with the sampled taxa covering all of the currently recognized subfamilies. The monophyly of Scutelleridae was confirmed by the congruence of the results of analyses conducted using Bayesian inference, maximum likelihood and maximum parsimony. The phylogenetic relationships among subfamilies were well resolved for the first time. Furthermore, time‐divergence studies estimated that the time of origin of Scutelleridae was in the Early Cretaceous (142.1–122.8 Ma), after the origin of the angiosperms. The diversification between the extant subfamilies of Scutelleridae and within the subfamilies occurred from the late Palaeocene to the late Miocene, simultaneously with the rise of the major groups of angiosperms and other phytophagous insects.     

The complete mitochondrial genome and novel gene arrangement of the unique-headed bug Stenopirates sp. (Hemiptera: Enicocephalidae)

Many of true bugs are important insect pests to cultivated crops and some are important vectors of human diseases, but few cladistic analyses have addressed relationships among the seven infraorders of Heteroptera. The Enicocephalomorpha and Nepomorpha are consider the basal groups of Heteroptera, but the basal-most lineage remains unresolved. Here we report the mitochondrial genome of the unique-headed bug Stenopirates sp., the first mitochondrial genome sequenced from Enicocephalomorpha. The Stenopirates sp. mitochondrial genome is a typical circular DNA molecule of 15, 384 bp in length, and contains 37 genes and a large non-coding fragment. The gene order differs substantially from other known insect mitochondrial genomes, with rearrangements of both tRNA genes and protein-coding genes. The overall AT content (82.5%) of Stenopirates sp. is the highest among all the known heteropteran mitochondrial genomes. The strand bias is consistent with other true bugs with negative GC-skew and positive AT-skew for the J-strand. The heteropteran mitochondrial atp8 exhibits the highest evolutionary rate, whereas cox1 appears to have the lowest rate. Furthermore, a negative correlation was observed between the variation of nucleotide substitutions and the GC content of each protein-coding gene. A microsatellite was identified in the putative control region. Finally, phylogenetic reconstruction suggests that Enicocephalomorpha is the sister group to all the remaining Heteroptera.     

Characteristics of the sperm structure in heteroptera (Hemiptera,Insecta)

Spermatozoa from eight heteropterans, each representing a different family, have been examined by electron microscopy in order to determine whether there exist characters typical for this insect group. Two such characters were found, namely bridges from the mitochondrial derivatives to the axonemal microtubules nos. 1 and 5, and two or three, rather than one, crystalline bodies within the mitochondrial derivatives. It is suggested that these characters are synapomorphic traits. The heteropteran spermatozoa lack accessory bodies typical of spermatozoa from many related groups of insects. The acrosome of the aquatic or semi-aquatic heteropterans (the infraorders Nepomorpha and Gerromorpha) has a peculiar inner structure consisting of tightly packed tubules. On the common theme of the heteropteran sperm structure, there were many variations, and the spermatozoa of each species examined can be recognized.     

Structure of aquatic assemblages of Coleoptera and Heteroptera in relation to habitat type and flood dynamic structure

The abundance and taxonomic composition of the aquatic insect fauna were investigated, with focus on adult water bugs, water beetles and water scavenger beetles (Heteroptera: Nepomorpha and Gerromorpha, and Coleoptera: Hydradephaga and Hydrophilidae) in two different freshwater habitats: (1) a periodically flooded area of the Special Zoological Reserve in Kopa?ki rit Nature Park, Croatia; and (2) melioration canals in the wider area of the Nature Park during 2005. Aquatic insects are generally abundant in various water systems, including floodplains that are exposed to water level fluctuations. Our aims were (1) to determine abundance and species richness in relation to habitat type; (2) to determine the influence of high flood peaks and oscillations during high water levels on the diversity of aquatic Coleoptera and Heteroptera in the flooded area; and (3) to identify characteristic species associated with each habitat type. We collected 71 species; 41 were captured at canals and 64 at the flooded area. Diversity of the two habitat types varied depending on the months but there were remarkable differences in species pool and their abundance. Both high and low water levels as well as oscillations during high water levels had major influence on species assemblages at the flooded area. Diversity of aquatic Coleoptera and Heteroptera was higher when the water level decreased after high water level peaks. A total of 11 species fulfilled the criteria for specificity and were sufficiently abundant to be suitable species characteristic for these two habitats. A higher proportion of significant characteristic species was present in the flooded area than in the canals. The presence of two Red List species of water beetles (Graphoderus bilineatus De Geer, 1774 and Berosus geminus Reiche et Saulcy, 1856) and nine significant characteristic species at the flooded area clearly indicates that the contribution of floodplains in maintaining freshwater biodiversity is not only important regionally but also at the international level. Also, our results suggest that the power of high water levels is an important factor that can be used in analyses on aquatic Coleoptera and Heteroptera assemblages, showing the uniqueness of large floodplain areas.     

Mitochondrial genomes advance phylogenetic hypotheses for Tylenchina (Nematoda: Chromadorea)

Within the nematode class Chromadorea, the suborder Tylenchina is an ecologically and morphologically diverse assemblage of nematodes that includes free‐living microbivores, fungivores and various types of plant parasites. A recent nematode classification system based largely on SSU rDNA phylogenetic trees classified suborder Tylenchina to include four infraorders: Panagrolaimomorpha, Cephalobomorpha, Tylenchomorpha and Drilonematomorpha, and phylogenetic relationships among species of these infraorders have not always been robustly supported. In this study, we determined the complete mitochondrial genome sequences of three Tylenchina species (Aphelenchus avenae [Aphelenchidae, Tylenchomorpha], Halicephalobus gingivalis, Panagrellus redivivus [Panagrolaimomorpha]) and the partial genome sequence of Acrobeles complexus (Cephalobomorpha) and used these sequences to infer phylogenetic relationships among representatives of the Tylenchina and other nematodes. Phylogenetic analysis of amino acid sequences for 12 protein‐coding genes of 100 nematode species supports monophyly of: Chromadorea, Spiruromorpha, Oxyuridomorpha, Ascarididae + Toxocaridae + Anisakidae, Meloidogynidae + Pratylenchidae + Heteroderidae and Aphelenchoidea. Bayesian and maximum‐likelihood analyses also show the nested position of Diplogasteromorpha within Rhabditomorpha, and Rhigonematomorpha within Ascaridomorpha. These analyses also show non‐monophyly of: clade III, Ancylostomatidae, Panagrolaimomorpha, Tylenchina and Tylenchomorpha. Reconstructed mitochondrial genome phylogeny also revealed that among two main Tylenchomorpha groups, the monophyletic group representing Aphelenchoidea species was sister to the large clade consisting of Ascaridomorpha, Diplogasteromorpha, Rhabditomorpha and Rhigonematomorpha and some Panagrolaimomorpha species, whereas Tylenchoidea species were sister to the most inclusive assemblage containing all infraordinal groups of Chromadorea, except for P. redivivus (Panagrolaimomorpha) and Acrobeles complexus (Cephalobomorpha). The monophyly of Aphelenchoidea (i.e. sister relationship between Aphelenchidae and Aphelenchoididae) recovered in this study indicates that similarity in certain aspects of pharyngeal structure between these two families appears best explained by common ancestry, rather than convergent evolution.     

Aquatic heteroptera from Mariana County, Minas Gerais, Brazil

In surveys carried out in lotic and lentic environments in Mariana County, Minas Gerais state, Brazil, 35 genera and 64 species of aquatic and semi-aquatic Heteroptera were recorded, distributed in 13 families. Thirty four species were collected in lentic environments, while in lotic environments 48 species were collected, some of them common to both environments. Nepomorpha presented the greatest number of species (45), markedly for the family Naucoridae, represented by 12 species. Among the 19 Gerromorpha species collected, eight were Veliidae and six were Gerridae.     

Flood pulses drive the temporal dynamics of assemblages of aquatic insects (Heteroptera and Coleoptera) in a temperate floodplain

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Model-based multi-locus estimation of decapod phylogeny and divergence times

Phylogenetic relationships among all of the major decapod infraorders have never been estimated using molecular data, while morphological studies produce conflicting results. In the present study, the phylogenetic relationships among the decapod basal suborder Dendrobranchiata and all of the currently recognized decapod infraorders within the suborder Pleocyemata (Caridea, Stenopodidea, Achelata, Astacidea, Thalassinidea, Anomala, and Brachyura) were inferred using 16S mtDNA, 18S and 28S rRNA, and the histone H3 gene. Phylogenies were reconstructed using the model-based methods of maximum likelihood and Bayesian methods coupled with Markov Chain Monte Carlo inference. The phylogenies revealed that the seven infraorders are monophyletic, with high clade support values (bp>70; pP>0.95) under both methods. The two suborders also were recovered as monophyletic, but with weaker support (bp=70; pP=0.74). Although the nodal support values for infraordinal relationships were low (bp<50; pP<0.77) the Anomala and Brachyura were basal to the rest of the 'Reptantia' in both reconstructions and using Bayesian tree topology tests alternate morphology-based hypotheses were rejected (P<0.01). Newly developed multi-locus Bayesian and likelihood heuristic rate-smoothing methods to estimate divergence times were compared using eight fossil and geological calibrations. Estimated times revealed that the Decapoda originated earlier than 437MYA and that the radiation within the group occurred rapidly, with all of the major lineages present by 325MYA. Node time estimation under both approaches is severely affected by the number and phylogenetic distribution of the fossil calibrations chosen. For analyses incorporating fossils as fixed ages, more consistent results were obtained by using both shallow and deep or clade-related calibration points. Divergence time estimation using fossils as lower and upper limits performed well with as few as one upper limit and a single deep fossil lower limit calibration.