Molecular phylogeny, historical biogeography and revised classification of andrenine bees (Hymenoptera: Andrenidae).

The mining bee subfamily Andreninae (Hymenoptera: Andrenidae) is a widely distributed and diverse group of ground-nesting solitary bees, including numerous species known to be important pollinators. Most of the species diversity of Andreninae is concentrated in the mainly Holarctic genus Andrena, comprising ca. 1550 described species. The subfamily and especially the genus have remained relatively neglected by recent molecular phylogenetic studies, with current classifications relying largely on morphological characters. We sampled ultraconserved element (UCE) sequences from 235 taxa, including all andrenine genera and 98 out of 104 currently recognized Andrena subgenera. Using 419,858 aligned nucleotide sites from 1009 UCE loci, we present a comprehensive molecular phylogenetic analysis of the subfamily. Our analysis supports the recognition of seven distinct genera in the Andreninae: Alocandrena, Ancylandrena, Andrena, Cubiandrena, Euherbstia, Megandrena, and Orphana. Within the genus Andrena, present-day subgeneric concepts revealed high degrees of paraphyly and polyphyly, due to strong homoplasy of morphological characters, necessitating a thorough, extensive revision of the higher classification of the genus. Based on our findings, we place the subgenus Calcarandrena in synonymy with Andrena (Lepidandrena); Hyperandrena, Nemandrena, Scoliandrena, Tylandrena and Zonandrena with A. (Melandrena); Distandrena, Fumandrena and Proxiandrena with A. (Micrandrena); Carandrena with A. (Notandrena); Agandrena with A. (Plastandrena); Geandrena and Xanthandrena with A. (Ptilandrena); Xiphandrena with A. (Scrapteropsis); and Platygalandrena and Poliandrena with A. (Ulandrena) (new synonymies). We additionally reestablish the groups known as Opandrena and Truncandrena as valid subgenera of Andrena. Our results also show that the MRCA of Andrena + Cubiandrena dispersed from the New World to the Palaearctic probably during the Eocene-early Oligocene, followed by 10-14 Neogene dispersal events from the Palaearctic to the Nearctic and 1-6 Neogene dispersals back into the Palaearctic, all within the genus Andrena.

Twenty-five new species of mining bees (Hymenoptera: Andrenidae: Andrena) from Israel and the Levant.

Andrena is one of the most diverse bee genera, comprising about 1,600 described species of ground-nesting solitary bees. Many Andrena species are plant specialists, and several taxa have been indicated to be important pollinators of wild and/or crop plants. The Eastern Mediterranean Basin and Israel in particular are one of the main world diversity hotspots of Andrena. Based on extensive examination of museum specimens combined with DNA barcoding, we hereby describe twenty-five Levantine species of Andrena new to science: Andrena anathema Pisanty sp. nov., A. ardentia Pisanty sp. nov., A. asluji Pisanty sp. nov., A. curviocciput Pisanty & Wood sp. nov., A. dividicincta Pisanty sp. nov., A. dorchini Pisanty sp. nov., A. euphorbiae Pisanty sp. nov., A. gageae Wood & Pisanty sp. nov., A. herodesi Pisanty & Wood sp. nov., A. hulae Pisanty sp. nov., A. igraeca Pisanty & Wood sp. nov., A. inusitata Pisanty sp. nov., A. janthinoides Pisanty sp. nov., A. longistilus Pisanty & Wood sp. nov., A. lunaris Pisanty & Wood sp. nov., A. macula Pisanty & Wood sp. nov., A. obtusa Pisanty sp. nov., A. ornithogali Pisanty & Wood sp. nov., A. petrae Wood sp. nov., A. protuber Pisanty sp. nov., A. sulfurea Wood sp. nov., A. turmalina Pisanty & Wood sp. nov., A. veronicae Pisanty & Wood sp. nov., A. veterana Pisanty sp. nov., and A. xera Pisanty sp. nov. We synonymise Andrena edentula Wood with A. tadauchii Gusenleitner syn. nov., and recognise four infraspecific names as valid species: Andrena mediterranea Pisanty & Scheuchl stat. nov., A. mizorhina Warncke stat. nov., A. noacki Alfken sp. resurr. and A. ochraceohirta Alfken sp. resurr. We additionally describe the hitherto unknown sexes of four species, provide new records for fifteen species previously unknown from Israel, and list fourteen taxa whose previously reported presence in Israel is considered erroneous or questionable.

The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila).

Over 22,000 species of biotically pollinated flowering plants, including some major agricultural crops, depend primarily on bees capable of floral sonication for pollination services. The ability to sonicate ("buzz") flowers is widespread in bees but not ubiquitous. Despite the prevalence of this pollinator behavior and its importance to natural and agricultural systems, the evolutionary history of floral sonication in bees has not been previously studied. Here, we reconstruct the evolutionary history of floral sonication in bees by generating a time-calibrated phylogeny and reconstructing ancestral states for this pollen extraction behavior. We also test the hypothesis that the ability to sonicate flowers and thereby efficiently access pollen from a diverse assemblage of plant species, led to increased diversification among sonicating bee taxa. We find that floral sonication evolved on average 45 times within bees, possibly first during the Early Cretaceous (100-145 million years ago) in the common ancestor of bees. We find that sonicating lineages are significantly more species rich than nonsonicating sister lineages when comparing sister clades, but a probabilistic structured rate permutation on phylogenies approach failed to support the hypothesis that floral sonication is a key driver of bee diversification. This study provides the evolutionary framework needed to further study how floral sonication by bees may have facilitated the spread and common evolution of angiosperm species with poricidal floral morphology.

A review of unusual species of Cotesia (Hymenoptera, Braconidae, Microgastrinae) with the first tergite narrowing at midlength.

The unusual species of Cotesia (Hymenoptera, Braconidae, Microgastrinae) with the first tergite narrowing at midlength are reviewed. One new species, Cotesia trabalae sp. n. is described from India and compared with Cotesia pistrinariae (Wilkinson) from Africa, the only other species sharing the same character of all the described species worldwide. The generic placement of these two species, based on molecular and morphological analyses as well as parasitoid biology is discussed.

Review of Apanteles sensu stricto (Hymenoptera, Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica.

More than half a million specimens of wild-caught Lepidoptera caterpillars have been reared for their parasitoids, identified, and DNA barcoded over a period of 34 years (and ongoing) from Area de Conservación de Guanacaste (ACG), northwestern Costa Rica. This provides the world's best location-based dataset for studying the taxonomy and host relationships of caterpillar parasitoids. Among Hymenoptera, Microgastrinae (Braconidae) is the most diverse and commonly encountered parasitoid subfamily, with many hundreds of species delineated to date, almost all undescribed. Here, we reassess the limits of the genus Apanteles sensu stricto, describe 186 new species from 3,200+ parasitized caterpillars of hundreds of ACG Lepidoptera species, and provide keys to all 205 described Apanteles from Mesoamerica - including 19 previously described species in addition to the new species. The Mesoamerican Apanteles are assigned to 32 species-groups, all but two of which are newly defined. Taxonomic keys are presented in two formats: traditional dichotomous print versions and links to electronic interactive versions (software Lucid 3.5). Numerous illustrations, computer-generated descriptions, distributional information, wasp biology, and DNA barcodes (where available) are presented for every species. All morphological terms are detailed and linked to the Hymenoptera Anatomy Ontology website. DNA barcodes (a standard fragment of the cytochrome c oxidase I (COI) mitochondrial gene), information on wasp biology (host records, solitary/gregariousness of wasp larvae), ratios of morphological features, and wasp microecological distributions were used to help clarify boundaries between morphologically cryptic species within species-complexes. Because of the high accuracy of host identification for about 80% of the wasp species studied, it was possible to analyze host relationships at a regional level. The ACG species of Apanteles attack mainly species of Hesperiidae, Elachistidae and Crambidae (Lepidoptera). About 90% of the wasp species with known host records seem to be monophagous or oligophagous at some level, parasitizing just one host family and commonly, just one species of caterpillar. Only 15 species (9%) parasitize species in more than one family, and some of these cases are likely to be found to be species complexes. We have used several information sources and techniques (traditional taxonomy, molecular, software-based, biology, and geography) to accelerate the process of finding and describing these new species in a hyperdiverse group such as Apanteles. The following new taxonomic and nomenclatural acts are proposed. Four species previously considered to be Apanteles are transferred to other microgastrine genera: Dolichogenidea hedyleptae (Muesebeck, 1958), comb. n., Dolichogenidea politiventris (Muesebeck, 1958), comb. n., Rhygoplitis sanctivincenti (Ashmead, 1900), comb. n., and Illidops scutellaris (Muesebeck, 1921), comb. rev. One European species that is a secondary homonym to a Mesoamerican species is removed from Apanteles and transferred to another genus: Iconella albinervis (Tobias, 1964), stat. rev. The name Apanteles albinervican Shenefelt, 1972, is an invalid replacement name for Apanteles albinervis (Cameron, 1904), stat. rev., and thus the later name is reinstated as valid. The following 186 species, all in Apanteles and all authored by Fernández-Triana, are described as species nova: adelinamoralesae, adrianachavarriae, adrianaguilarae, adrianguadamuzi, aichagirardae, aidalopezae, albanjimenezi, alejandromasisi, alejandromorai, minorcarmonai, alvarougaldei, federicomatarritai, anabellecordobae, rostermoragai, anamarencoae, anamartinesae, anapiedrae, anariasae, andreacalvoae, angelsolisi, arielopezi, bernardoespinozai, bernyapui, bettymarchenae, bienvenidachavarriae, calixtomoragai, carloscastilloi, carlosguadamuzi, eliethcantillanoae, carlosrodriguezi, carlosviquezi, carloszunigai, carolinacanoae, christianzunigai, cinthiabarrantesae, ciriloumanai, cristianalemani, cynthiacorderoae, deifiliadavilae, dickyui, didiguadamuzi, diegoalpizari, diegotorresi, diniamartinezae, duniagarciae, duvalierbricenoi, edgarjimenezi, edithlopezae, eduardoramirezi, edwinapui, eldarayae, erickduartei, esthercentenoae, eugeniaphilipsae, eulogiosequeira, felipechavarriai, felixcarmonai, fernandochavarriai, flormoralesae, franciscopizarroi, franciscoramirezi, freddyquesadai, freddysalazari, gabrielagutierrezae, garygibsoni, gerardobandoi, gerardosandovali, gladysrojasae, glenriverai, gloriasihezarae, guadaluperodriguezae, guillermopereirai, juanmatai, harryramirezi, hectorsolisi, humbertolopezi, inesolisae, irenecarrilloae, isaacbermudezi, isidrochaconi, isidrovillegasi, ivonnetranae, jairomoyai, javiercontrerasi, javierobandoi, javiersihezari, jesusbrenesi, jesusugaldei, jimmychevezi, johanvargasi, jorgecortesi, jorgehernandezi, josecalvoi, josecortesi, josediazi, josejaramilloi, josemonteroi, joseperezi, joserasi, juanapui, juancarrilloi, juangazoi, juanhernandezi, juanlopezi, juanvictori, juliodiazi, juniorlopezi, keineraragoni, laurahuberae, laurenmoralesae, leninguadamuzi, leonelgarayi, lilliammenae, lisabearssae, luciariosae, luisbrizuelai, luiscanalesi, luiscantillanoi, luisgarciai, luisgaritai, luishernandezi, luislopezi, luisvargasi, manuelarayai, manuelpereirai, manuelriosi, manuelzumbadoi, marcobustosi, marcogonzalezi, marcovenicioi, mariachavarriae mariaguevarae, marialuisariasae, mariamendezae, marianopereirai, mariatorrentesae, sigifredomarini, marisolarroyoae, marisolnavarroae, marvinmendozai, mauriciogurdiani, milenagutierrezae, monicachavarriae, oscarchavesi, osvaldoespinozai, pablotranai, pabloumanai, pablovasquezi, paulaixcamparijae, luzmariaromeroae, petronariosae, randallgarciai, randallmartinezi, raulacevedoi, raulsolorsanoi, wadyobandoi, ricardocaleroi, robertmontanoi, robertoespinozai, robertovargasi, rodrigogamezi, rogerblancoi, rolandoramosi, rolandovegai, ronaldcastroi, ronaldgutierrezi, ronaldmurilloi, ronaldnavarroi, ronaldquirosi, ronaldzunigai, rosibelelizondoae, ruthfrancoae, sergiocascantei, sergioriosi, tiboshartae, vannesabrenesae, minornavarroi, victorbarrantesi, waldymedinai, wilbertharayai, williamcamposi, yeissonchavesi, yilbertalvaradoi, yolandarojasae, hazelcambroneroae, zeneidabolanosae.

Origins, evolution, and diversification of cleptoparasitic lineages in long-tongued bees.

The evolution of parasitic behavior may catalyze the exploitation of new ecological niches yet also binds the fate of a parasite to that of its host. It is thus not clear whether evolutionary transitions from free-living organism to parasite lead to increased or decreased rates of diversification. We explore the evolution of brood parasitism in long-tongued bees and find decreased rates of diversification in eight of 10 brood parasitic clades. We propose a pathway for the evolution of brood parasitic strategy and find that a strategy in which a closed host nest cell is parasitized and the host offspring is killed by the adult parasite represents an obligate first step in the appearance of a brood parasitic lineage; this ultimately evolves into a strategy in which an open host cell is parasitized and the host offspring is killed by a specialized larval instar. The transition to parasitizing open nest cells expanded the range of potential hosts for brood parasitic bees and played a fundamental role in the patterns of diversification seen in brood parasitic clades. We address the prevalence of brood parasitic lineages in certain families of bees and examine the evolution of brood parasitism in other groups of organisms.

A review of the New World species of the parasitoid wasp Iconella (Hymenoptera, Braconidae, Microgastrinae).

The New World species of Iconella (Hymenoptera: Braconidae, Microgastrinae) are revised. Iconella andydeansi Fernández-Triana, sp. n., Iconella canadensis Fernández-Triana, sp. n., and Iconella jayjayrodriguezae Fernández-Triana, sp. n., are described as new. Iconella isolata (Muesebeck, 1955), stat. r., previously considered as a subspecies of Iconella etiellae (Viereck, 1911), is here elevated to species rank. All species have different, well defined geographic distributions and hosts. Taxonomic keys are presented in two formats: traditional dichotomous hardcopy versions and links to electronic interactive versions (software Lucid 3.5). Numerous illustrations, computer-generated descriptions, distributional information, host records (mostly Lepidoptera: Crambidae and Pyralidae), and DNA barcodes (where available) are presented for every species. Phylogenetic analyses of the barcoding region of COI indicate the possibility that Iconella is not monophyletic and that the New World species may not form a monophyletic group; more data is needed to resolve this issue.

Bees diversified in the age of eudicots.

Reliable estimates on the ages of the major bee clades are needed to further understand the evolutionary history of bees and their close association with flowering plants. Divergence times have been estimated for a few groups of bees, but no study has yet provided estimates for all major bee lineages. To date the origin of bees and their major clades, we first perform a phylogenetic analysis of bees including representatives from every extant family, subfamily and almost all tribes, using sequence data from seven genes. We then use this phylogeny to place 14 time calibration points based on information from the fossil record for an uncorrelated relaxed clock divergence time analysis taking into account uncertainties in phylogenetic relationships and the fossil record. We explore the effect of placing a hard upper age bound near the root of the tree and the effect of different topologies on our divergence time estimates. We estimate that crown bees originated approximately 123 Ma (million years ago) (113-132 Ma), concurrently with the origin or diversification of the eudicots, a group comprising 75 per cent of angiosperm species. All of the major bee clades are estimated to have originated during the Middle to Late Cretaceous, which is when angiosperms became the dominant group of land plants.

The impact of molecular data on our understanding of bee phylogeny and evolution.

Our understanding of bee phylogeny has improved over the past fifteen years as a result of new data, primarily nucleotide sequence data, and new methods, primarily model-based methods of phylogeny reconstruction. Phylogenetic studies based on single or, more commonly, multilocus data sets have helped resolve the placement of bees within the superfamily Apoidea; the relationships among the seven families of bees; and the relationships among bee subfamilies, tribes, genera, and species. In addition, molecular phylogenies have played an important role in inferring evolutionary patterns and processes in bees. Phylogenies have provided the comparative framework for understanding the evolution of host-plant associations and pollen specialization, the evolution of social behavior, and the evolution of parasitism. In this paper, we present an overview of significant discoveries in bee phylogeny based primarily on the application of molecular data. We review the phylogenetic hypotheses family-by-family and then describe how the new phylogenetic insights have altered our understanding of bee biology.

Mariapanteles (Hymenoptera, Braconidae), a new genus of Neotropical microgastrine parasitoid wasp discovered through biodiversity inventory.

A new genus of microgastrine parasitoid wasps, Mariapanteles Whitfield & Fernández-Triana, gen. n., is described from rain forests of the Neotropics. The new genus is related to the common and speciose genus Pseudapanteles, but can be distinguished from the latter by having a complete transverse carina on the propodeum which forks around the spiracles. A molecular analysis based on data from COI from specimens of the proposed new genus plus possibly related genera confirms its generic distinctness. A key to two known species, Mariapanteles felipei Whitfield, sp. n. (Costa Rica) and Mariapanteles dapkeyae Fernández-Triana, sp. n. (Brazil) is provided. Evidence from collections suggests that there are other undescribed Neotropical congenerics. Specimens of Mariapanteles were likely confused in the past with the genus Beyarslania (referred to as Xenogaster until recently) but present information suggests that Beyarslania is restricted to the Afrotropical region while the Neotropical species clearly belong to a different genus, which we propose as new.

The antiquity and evolutionary history of social behavior in bees.

A long-standing controversy in bee social evolution concerns whether highly eusocial behavior has evolved once or twice within the corbiculate Apidae. Corbiculate bees include the highly eusocial honey bees and stingless bees, the primitively eusocial bumble bees, and the predominantly solitary or communal orchid bees. Here we use a model-based approach to reconstruct the evolutionary history of eusociality and date the antiquity of eusocial behavior in apid bees, using a recent molecular phylogeny of the Apidae. We conclude that eusociality evolved once in the common ancestor of the corbiculate Apidae, advanced eusociality evolved independently in the honey and stingless bees, and that eusociality was lost in the orchid bees. Fossil-calibrated divergence time estimates reveal that eusociality first evolved at least 87 Mya (78 to 95 Mya) in the corbiculates, much earlier than in other groups of bees with less complex social behavior. These results provide a robust new evolutionary framework for studies of the organization and genetic basis of social behavior in honey bees and their relatives.

Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism.

Apidae is the most speciose and behaviorally diverse family of bees. It includes solitary, eusocial, socially parasitic, and an exceptionally high proportion of cleptoparasitic species. Cleptoparasitic bees, which are brood parasites in the nests of other bees, have long caused problems in resolving the phylogenetic relationships within Apidae based on morphological data because of the tendency for parasites to converge on a suite of traits, making it difficult to differentiate similarity caused by common ancestry from convergence. Here, we resolve the evolutionary history of apid cleptoparasitism by conducting a detailed, comprehensive molecular phylogenetic analysis of all 33 apid tribes (based on 190 species), including representatives from every hypothesized origin of cleptoparasitism. Based on Bayesian ancestral state reconstruction, we show that cleptoparasitism has arisen just four times in Apidae, which is fewer times than previously estimated. Our results indicate that 99% of cleptoparasitic apid bees form a monophyletic group. Divergence time estimates reveal that cleptoparasitism is an ancient behavior in bees that first evolved in the late Cretaceous 95 Mya [95% highest posterior density (HPD) = 87-103]. Our phylogenetic analysis of the Apidae sheds light on the macroevolution of a bee family that is of evolutionary, ecological, and economic importance.

Phylogenetic analysis of the corbiculate Apinae based on morphology of the sting apparatus (Hymenoptera: Apidae).

This study aimed to test the various competing hypotheses regarding the relationships among the four tribes of corbiculate apine bees (Euglossini "orchid bees", Bombini "bumble bees", Meliponini "stingless bees", and Apini "honey bees") with a completely new set of previously unstudied morphological characters derived from the sting apparatus. The result was one most parsimonious tree of 49 steps, CI = 89, RI = 93 that is perfectly congruent with most studies based on morphological and combined morphological/molecular data, i.e., Euglossini + (Bombini + (Meliponini + Apini)), supporting a well accepted scenario of social evolution for these bees. This data matrix was then combined with other published matrices for this group in order to perform simultaneous analyses. The problem of how to best combine the multiple matrices that did not use the same exemplars was investigated.