Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an emphasis on the superfamily Apoidea

Debevec, AH., Cardinal, S & Danforth, BN. Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an emphasis on the superfamily Apoidea. —Zoologica Scripta, 41, 527–535. The hymenopteran superfamily Apoidea includes the bees (Anthophila) as well as four predatory wasp families (Heterogynaidae, Ampulicidae, Sphecidae and Crabronidae) collectively referred to as the “sphecoid” or “apoid” wasps. The most widely cited studies suggest that bees are sister to the wasp family Crabronidae, but alternative hypotheses have been proposed based on both morphological and molecular data. We combined DNA sequence data from previously published studies and newly generated data for four nuclear genes (28S, long‐wavelength rhodopsin, elongation factor‐1α and wingless) to identify the likely sister group to the bees. Analysis of our four‐gene data set by maximum likelihood and Bayesian methods indicates that bees most likely arise from within a paraphyletic Crabronidae. Possible sister groups to the bees include Philanthinae, Pemphredoninae or Philanthinae + Pemphredoninae. We used Bayesian methods to explore the robustness of our results. Bayes Factor tests strongly rejected the hypotheses of crabronid monophyly as well as placement of Heterogynaidae within Crabronidae. Our results were also stable to alternative rootings of the bees. These findings provide additional support for the hypothesis that bees arise from within Crabronidae, rather than being sister to Crabronidae, thus altering our understanding of bee ancestry and evolutionary history.     

A molecular phylogeny for digger wasps in the tribe Ammophilini (Hymenoptera,Apoidea, Sphecidae)

The evolution of parental care strategies in aculeate (stinging) wasps and bees has been much studied from a functional perspective, but relatively little phylogenetic information is available to place this in a rigorous historical context, especially at the species level. We used mitochondrial cytochrome oxidase I and two nuclear genes, the elongation factor‐1α and LW rhodopsin, to investigate the phylogeny of Sphecidae digger wasps. We focus particularly on the tribe Ammophilini, a clade of nonsocial apoid wasps that exhibit unusually diverse parental care strategies. We analysed a 2232 bp dataset for 40 ammophilines plus nine other taxa from within the remaining Sphecidae. Our Bayesian phylogeny provides strong support for the monophyly of Ammophilini and for the monophyly of all six individual ammophiline genera, except that the position of P. affinis within the genus Podalonia is only weakly supported. The monophyly of some, but not all, previously designated species groups within the genus Ammophila is supported. We discuss the implications of our results for the evolution of morphological traits used previously in ammophiline systematics.     

Single-copy nuclear genes recover cretaceous-age divergences in bees

We analyzed the higher level phylogeny of the bee family Halictidae based on the coding regions of three single-copy nuclear genes (long-wavelength [LW] opsin, wingless, and elongation factor 1-alpha [EF-1 alpha]). Our combined data set consisted of 2,234 aligned nucleotide sites (702 base pairs [bp] for LW opsin, 405 bp for wingless, and 1,127 bp for EF-1 alpha) and 779 parsimony-informative sites. We included 58 species of halictid bees from 33 genera, representing all subfamilies and tribes, and rooted the trees using seven outgroups from other bee families: Colletidae, Andrenidae, Melittidae, and Apidae. We analyzed the separate and combined data sets by a variety of methods, including equal weights parsimony, maximum likelihood, and Bayesian methods. Analysis of the combined data set produced a strong phylogenetic signal with high bootstrap and Bremer support and high posterior probability well into the base of the tree. The phylogeny recovered the monophyly of the Halictidae and of all four subfamilies and both tribes, recovered relationships among the subfamilies and tribes congruent with morphology, and provided robust support for the relationships among the numerous genera in the tribe Halictini, sensu Michener (2000). Using our combined nucleotide data set, several recently described halictid fossils from the Oligocene and Eocene, and recently developed Bayesian methods, we estimated the antiquity of major clades within the family. Our results indicate that each of the four subfamilies arose well before the Cretaceous-Tertiary boundary and suggest that the early radiation of halictid bees involved substantial African-South American interchange roughly coincident with the separation of these two continents in the late Cretaceous. This combination of single-copy nuclear genes is capable of recovering Cretaceous-age divergences in bees with high levels of support. We propose that LW opsin, wingless, and EF-1 alpha(F2 copy) may be useful in resolving relationships among bee families and other Cretaceous-age insect lineages.     

Phylogenetic utility of the major opsin in bees (Hymenoptera: Apoidea): a reassessment

Major opsin (LW Rh) DNA sequence has been reported to provide useful data for resolving phylogenetic relationships among tribes of corbiculate bees based on analyses of 502 bp of coding sequence. However, the corbiculate tribes are believed to be of Cretaceous age, and strong support for insect clades of this age from small data sets of nucleotide sequence data has rarely been demonstrated. To more critically assess opsin's phylogenetic utility we generated an expanded LW Rh data set by sequencing the same gene fragment from 52 additional bee species from 24 tribes and all six extant bee families. Analyses of this data set failed to provide substantial support for monophyly of corbiculate bees, for relationships among corbiculate tribes, or for most other well-established higher-level relationships among long-tongued bees. However, monophyly of nearly all genera and tribes is strongly supported, indicating that LW Rh provides useful phylogenetic signal at lower taxonomic levels. When our expanded LW Rh data set is combined with a morphological and behavioral data set for corbiculate bees, the results unambiguously support the traditional phylogeny of the corbiculate bee tribes: (Euglossini + (Bombini + (Meliponini + Apini))). This implies a single origin of advanced eusocial behavior among bees rather than dual origins, as proposed by several recent studies.     

Green lacewing phylogeny, based on three nuclear genes (Chrysopidae, Neuroptera)

Abstract.  Systematic relationships among higher taxa within Chrysopidae, a large and agriculturally significant neuropteran family, are poorly understood. A molecular phylogenetic survey of Chrysopidae was performed with three nuclear genes, namely wingless (546 bp), phosphoenolpyruvate carboxykinase (483 bp), and sodium/potassium ATPase alpha subunit (410 bp). We examined 83 species in 24 genera, mainly from Japan, Eurasia and Africa. Parsimony and Bayesian analyses of combined datasets of a total of 1439 bp demonstrated that (1) monophyly of the subfamily Chrysopinae was supported but the relationship between Nothochrysinae and Apochrysinae was unclear, although the two subfamilies together may constitute the sister taxon of Chrysopinae; (2) of the three tribes examined within Chrysopinae (Ankylopterygini, Belonopterygini and Chrysopini), monophyly of Ankylopterygini and Belonopterygini was supported, but the relationships among the three remain unclear; (3) seven sub-clades in Chrysopini were indicated, namely (i) Brinckochrysa , (ii) Chrysemosa  +  Suarius , (iii) Chrysotropia  +  Nineta , (iv) Mallada  +  Chrysoperla  +  Peyerimhoffina , (v) Cunctochrysa  +  Meleoma  +  Nipponochrysa  +  Apertochrysa albolineatoides , (vi) Chrysopa  +  Plesiochrysa , and (vii) Dichochrysa  +  Apertochrysa eurydera ; and (4) most genera were monophyletic, except for Apertochrysa and Cunctochrysa , each of which was shown to have two distinct origins. Our molecular analysis allowed the assignment of several species of uncertain affinities to known genera. There was some disagreement between the molecular and previously published morphological phylogenies, but in general our results confirmed existing morphological hypotheses of evolution within the family.     

DNA barcodes identify 99 per cent of apoid wasp species (Hymenoptera: Ampulicidae,Crabronidae, Sphecidae) from the Western Palearctic

The apoid wasps have traditionally been regarded as a paraphyletic assemblage of four families (Ampulicidae, Crabronidae, Heterogynaidae and Sphecidae) that are closely related to the bees (Anthophila). The present study covers the three families of apoid wasps known to occur in Europe, that is, the Ampulicidae, Crabronidae and Sphecidae. DNA barcode sequences of 3,695 specimens of apoid wasps were analysed for the present study, including 21 specimens of Ampulicidae, 3,398 Crabronidae and 276 Sphecidae. The sequences of the dataset represent 661 species of apoid wasps, including two species of Ampulicidae, 613 of Crabronidae and 46 species of Sphecidae. The dataset includes DNA barcodes of 240 species of German apoid wasps, representing 88% of the German fauna, and 578 European species, representing 65% of the European apoid wasp fauna. The study demonstrates that virtually all species of the three examined families can be reliably identified by DNA barcodes. The implications of highly congruent results between traditional taxonomy and DNA barcoding for the reliable application of DNA‐based identifications are discussed.     

The major opsin in bees (Insecta: Hymenoptera): A promising nuclear gene for higher level phylogenetics.

We report the phylogenetic utility of the nuclear gene encoding the long-wavelength opsin (LW Rh) for tribes of bees. Aligned nucleotide sequences were examined in multiple taxa from the four tribes comprising the corbiculate bees within the subfamily Apinae. Phylogenetic analyses of sequence variation in a 502-bp fragment (approx 40% of the coding region) strongly supported the monophyly of each of the four tribes, which are well established from previous studies of morphology and DNA. Trees estimated from parsimony and maximum likelihood analyses of LW Rh sequences show a strongly supported relationship between the tribes Meliponini and Bombini, a relationship that has been found uniformly in studies of other genes (28S, 16S, and cytochrome b). All of the tribal clades as well as relationships among the tribes are supported by high bootstrap values, suggesting the utility of LW Rh in estimating tribal and subfamily rank for these bees. The sequences exhibit minimal base composition bias. Both 1st + 2nd and 3rd position sites provide information for estimating a reliable tree topology. These results suggest that LW Rh, which has not been reported previously in studies of organismal phylogenetics, could provide important new data from the nuclear genome for phylogeny reconstruction.     

Australian Lasioglossum + Homalictus form a monophyletic group: resolving the "Australian enigma"

The bee genus Lasioglossum includes > 1,000 species of bees distributed on all continents except Antarctica. Lasioglossum is a major component of the bee fauna in the Holarctic, Ethiopian, and Asian regions and is an important group for investigating the evolution of social behavior in bees. Given its cosmopolitan distribution, the historical biogeography of the genus is of considerable interest. We reconstructed phylogenetic relationships among the subgenera and species within Lasioglossum s.s., using DNA sequence data from a slowly evolving nuclear gene, elongation factor-1 alpha. The entire data set includes > 1,604 aligned nucleotide sites (including three exons plus two introns) for 89 species (17 outgroups plus 72 ingroups). Parsimony and maximum likelihood analyses provide strong evidence that the primarily Indoaustralian subgenera (Homalictus, Chilalictus, Parasphecodes) form a monophyletic group. Bootstrap support for the Australian clade ranged from 73% to 77%, depending on the method of analysis. Monophyly of the Australian Lasioglossum suggests that a single colonization event (by way of Southeast Asia and New Guinea) gave rise to a lineage of > 350 native Indoaustralian bees. We discuss the implications of Australian monophyly for resolving the "Australian enigma"--the similarity in social behavior among the Australian halictine bees relative to that of Holarctic groups.     

A comprehensive phylogeny of the bumble bees (Bombus)

Bumble bees ( Bombus Latreille) occupy a wide diversity of habitats, from alpine meadows to lowland tropical forest, yet they appear to be similar in morphology throughout their range, suggesting that behavioural adaptations play a more important role in colonizing diverse habitats. Notwithstanding their structural homogeneity, bumble bees exhibit striking inter- and intraspecific variation in colour pattern, purportedly the outcome of mimetic evolution. A robust phylogeny of Bombus would provide the framework for elucidating the history of their wide biogeographical distribution and the evolution of behavioural and morphological adaptations, including colour pattern. However, morphological studies of bumble bees have discovered too few phylogenetically informative characters to reconstruct a robust phylogeny. Using DNA sequence data, we report the first nearly complete species phylogeny of bumble bees, including most of the 250 known species from the 38 currently recognized subgenera. Bayesian analysis of nuclear (opsin, EF-1α, arginine kinase, PEPCK) and mitochondrial (16S) sequences results in a highly resolved and strongly supported phylogeny from base to tips, with clear-cut support for monophyly of most of the conventional morphology-based subgenera. Most subgenera fall into two distinct clades ( short-faced and long-faced ) associated broadly with differences in head morphology. Within the short-faced clade is a diverse New World clade, which includes nearly one-quarter of the currently recognized subgenera, many of which are restricted to higher elevations of Central and South America. The comprehensive phylogeny provides a firm foundation for reclassification and for evaluating character evolution in the bumble bees.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 161–188.     

New fossil evidence of the early diversification of bees: Paleohabropoda oudardi from the French Paleocene (Hymenoptera, Apidae, Anthophorini)

Phylogenetic relationships among and within the major groups of bees (Apoidea Apiformes) were recently reconsidered using extensive molecular and morphological datasets. The next step in the study of bee evolution will consist in estimating the antiquity of the nodes within the inferred topologies. We describe here the third oldest bee fossil, Paleohabropoda oudardi gen. n. sp. N. (Apidae, Apinae, Anthophorini) from the Paleocene of Menat (France, Puy-de-Dôme; 60 Myr). Phylogenetic analysis of 17 morphological characters and morphometric analysis of the wing shape were used to recover, respectively, its taxonomic position and morphological affinities. Our results indicate that Paleohabropoda oudardi gen. n. sp. n. clearly belongs to the Anthophorini. Paleohabropoda is therefore the oldest fossil that can be confidently date and place to an extant tribe. Its wing shape is surprisingly close to the extant genus Habropoda . The discovery of Paleohabropoda oudardi gen. n., sp. n. brings further evidence for the Cretaceous diversification of major lineages of bees and for strong constancy of wing shape within the Anthophorini.     

Wild bees (Hymenoptera: Apoidea) in an urban botanical garden in Buenos Aires,Argentina

We assessed bee diversity and abundance in a botanical garden in the city of Buenos Aires during two consecutive spring–summer periods. Every 15 days, we collected by hand-netting bee specimens seen foraging on flowers during five-minute censuses at every entomophilous herbaceous plant. A total of 66 bee species (Hymenoptera: Apoidea) were recorded. Richness and abundance of native, generalist, and above-ground nesting (cavities) species were higher than that of exotic, specialist, and below-ground (soil) nesting ones, respectively. Social bees were more abundant, while the richness of solitary species was higher than that of social bees. Cleptoparasitic species were represented by a high number of species, even though only a few individuals were captured. Our results suggest that the studied area is an important bee reservoir within the city.     

Systematics, phylogeny and biogeography of Anterastes (Orthoptera, Tettigoniidae, Tettigoniinae): evolution within a refugium

Çıplak, B. (2004). Systematics, phylogeny and biogeography of Anterastes (Orthoptera, Tettigoniidae, Tettigoniinae): evolution within a refugium. — Zoologica Scripta , 33 , 19–44.
The genus Anterastes , distributed in southeastern Europe and the western part of Anatolia, is revised based on previous materials and numerous specimens collected from new localities. A key to all species is presented. Two new species, A. antitauricus sp. n. and A. ucari sp. n. are described. Anterastes akdaghensis Ramme is placed in synonymy with A. babadaghi Uvarov. Cladistic analysis confirmed the monophyly of Anterastes . The relationships among the species of Anterastes are: A. uludaghensis  + (( A. serbicus  +  A. burri  +  A. antitauricus sp. n.) + ( A. anatolicus  +  A. tolunayi  + ( A. niger  + ( A. babadaghi  +  A. turcicus  +  A. ucari sp. n.)))). The biogeography of the genus shows a correlation with its phylogeny. It is assumed that the genus arose from an ancestral stock in northwestern Anatolia in the Pliocene and the later range of this ancestral population expanded and contracted under the effects of the ice ages (glacial and interglacial periods, respectively). It is postulated that speciation within the genus, suggested by phylogenetic analysis, might have occurred when the range of ancestral populations expanded during glacial periods and contracted in subsequent warm periods. The present species may be the product of relict populations remaining in refugia at higher altitudes with alpine or subalpine vegetation in southern Anatolia.     

Early duplication and functional diversification of the opsin gene family in insects

Recent analysis of the complete mosquito Anopheles gambiae genome has revealed a far higher number of opsin genes than for either the Drosophila melanogaster genome or any other known insect. In particular, the analysis revealed an extraordinary opsin gene content expansion, whereby half are long wavelength-sensitive (LW) opsin gene duplicates. We analyzed this genomic data in relationship to other known insect opsins to estimate the relative timing of the LW opsin gene duplications and to identify "missing" paralogs in extant species. The inferred branching patterns of the LW opsin gene family phylogeny indicate at least one early gene duplication within insects before the emergence of the orders Orthoptera, Mantodea, Hymenoptera, Lepidoptera, and Diptera. These data predict the existence of one more LW opsin gene than is currently known from most insects. We tested this prediction by using a degenerate PCR strategy to screen the hymenopteran genome for novel LW opsin genes. We isolated two LW opsin gene sequences from each of five bee species, Bombus impatiens, B. terrestris, Diadasia afflicta, D. rinconis, and Osmia rufa, including 1.1 to 1.2 kb from a known (LW Rh1) and 1 kb from a new opsin gene (LW Rh2). Phylogenetic analysis suggests that the novel hymenopteran gene is orthologous to A. gambiae GPRop7, a gene that is apparently missing from D. melanogaster. Relative rate tests show that LW Rh2 is evolving at a slower rate than LW Rh1 and, therefore, may be a useful marker for higher-level hymenopteran systematics. Site-specific rate tests indicate the presence of several amino acid sites between LW Rh1 and LW Rh2 that have undergone shifts in selective constraints after duplication. These sites and others are discussed in relationship to putative structural and functional differences between the two genes.     

A preliminary detective survey of hymenopteran insects at Jazan Lake Dam Region,Southwest of Saudi Arabia

A preliminary detective survey for the hymenopteran insect fauna of Jazan Lake dam region, Southwest Saudi Arabia, was carried out for one year from January 2018 to January 2019 using mainly sweep nets and Malaise traps. The survey revealed the presence of three hymenopteran Superfamilies (Apoidea, Vespoidea and Evanioidea) representing 15 species belonging to 10 genera of 6 families (Apidae, Crabronidae, Sphecidae, Vespidae, Mutillidae, and Evaniidae). The largest number of species has belonged to the family Crabronidae is represented by 6 species under 2 genera. While the family Apidae, is represented by 2 species under 2 genera. Family Vespidae is represented by 2 species of one genus. While, the rest of the families Sphecidae, Mutillida, and Evaniidae each is represented by only one species and one genus each. Eleven species are predators, two species are pollinators and two species are parasitics. Note for each family was provided, and species was provided with synonyms and general and taxonomic remarks and their worldwide geographic distribution and information about their economic importance are also included. All species were photographed with dorsal and lateral views.     

Assessing species boundaries and evolutionary relationships in a group of south-western European species of Isotomurus (Collembola, Isotomidae) using allozyme data

In this study allozyme data were used to examine evolutionary relationships in the cosmopolitan collembolan genus Isotomurus . Fifty-six south-western European populations from 13 species were compared, with the aim of delimiting species boundaries and testing the robustness of the most frequently used morphological characters for species identification. Observed allozyme variability suggests that genetic differentiation is more pronounced than the amount of morphological variability among and within species. Convergence in models of pigmentation pattern may lead to erroneous taxonomic identification when this is the only feature used for species diagnosis. In this respect, this study confirms that diagnosis is greatly improved when assisted by biochemical or molecular analyses. Allozyme data have also been used to reconstruct evolutionary hypotheses for relationships at the species and population level. The monophyly of Isotomurus maculatus , I. unifasciatus , I. fucicolus , I. nebulosus and I. pseudopalustris was confirmed on molecular grounds. Conversely, the monophyly of I. ghibellinus and I. palustris was rejected, suggesting the presence of cryptic species.     

秦巴山区蜜蜂资源调查研究

介绍了发生于秦巴山区的蜜蜂物种 5 0种 ,隶属蜜蜂总科之 6科 19属 ;同时介绍了这些物种的发生区域 ,发生期和发生概况。现行研究结果对于揭示、保护、利用当地的蜜蜂资源具有积极的指导作用。     

Molecular phylogeography of Apalone spinifera (Reptilia, Trionychidae)

The molecular evaluation of morphologically based species delimitations of many herpetofauna has improved the understanding of evolutionary processes and the rigor of conservation efforts. Previous evidence for a deep lineage divide between south-eastern + northern subspecies of the softshell turtle Apalone spinifera ( A. s. aspera  +  A. s. hartwegi  +  A. s. spinifera ) and western subspecies ( A. s. pallida  +  A. s. emoryi  +  A. s. guadalupensis ) was re-examined with a broader sampling using mitochondrial and nuclear markers. The south-eastern + northern clade and the western clade maintained mitochondrial reciprocal monophyly. We molecularly confirmed a geographical boundary between these two clades in Oklahoma, and developed a phylogeographical hypothesis that invokes stream capture. We evaluated whether these mitochondrial lineages represent distinct species by surveying these clades for divergence at the nuclear intron R35 and two nuclear genes, Cmos and recombination activating gene 1 (RAG-1). The nuclear loci showed no phylogenetic resolution and only the nuclear intron exhibited significant nearest neighbour statistics. Taken together, the nuclear data suggest that taxonomic elevation of the two mitochondrial clades would be currently unjustified.     

Phylogeny of the holometabolous insect orders: molecular evidence

Phylogenetic relationships among the holometabolous insect orders were reconstructed using 18S ribosomal DNA data drawn from a sample of 182 taxa representing all holometabolous insect orders and multiple outgroups. Parsimony analysis supports the monophyly of all holometabolous insect orders except for Coleoptera and Mecoptera. Mecoptera is paraphyletic with respect to Siphonaptera, which is nested within Mecoptera. Coleoptera is scattered as a paraphyletic assemblage across the tree topology. These data support a monophyletic Halteria (Strepsiptera + Diptera), Amphiesmenoptera (Trichoptera + Lepidoptera), Neuropterida (Neuroptera + (Megaloptera + Raphidioptera)), but Antliophora (Halteria + Mecoptera + Siphonaptera) and Mecopterida (Antliophora + Amphiesmenoptera) are paraphyletic. The limitations of using 18S ribosomal DNA as the sole phylogenetic marker for reconstructing insect ordinal relationships are discussed.     

Premières données sur les Halictidae (Hymenoptera : Apoidea) de la région de Batna (Est algérien)

First data about Halictidae (Hymenoptera: Apoidea) in the región of Batna (Eastern Algeria) Investigations carried out on Halictidae bees in different localities in the region of Batna during the spring and summer seasons of 2009 and 2012 allowed the identification of 35 species; Lasioglossum musculum is reported for the first time in Algeria. The presence of Sphecodes puncticeps Thomson, 1870, a cleptoparasitic species, is confirmed. The flowers visited and the flight period of each species are noted.