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      Annotated and illustrated world checklist of Microgastrinae parasitoid wasps (Hymenoptera, Braconidae)

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          Abstract

          A checklist of world species of Microgastrinae parasitoid wasps (Hymenoptera: Braconidae) is provided. A total of 81 genera and 2,999 extant species are recognized as valid, including 36 nominal species that are currently considered as species inquirendae. Two genera are synonymized under Apanteles. Nine lectotypes are designated. A total of 318 new combinations, three new replacement names, three species name amendments, and seven species status revised are proposed. Additionally, three species names are treated as nomina dubia, and 52 species names are considered as unavailable names (including 14 as nomina nuda). A total of three extinct genera and 12 extinct species are also listed. Unlike in many previous treatments of the subfamily, tribal concepts are judged to be inadequate, so genera are listed alphabetically. Brief diagnoses of all Microgastrinae genera, as understood in this paper, are presented. Illustrations of all extant genera (at least one species per genus, usually more) are included to showcase morphological diversity. Primary types of Microgastrinae are deposited in 108 institutions worldwide, although 76% are concentrated in 17 collections. Localities of primary types, in 138 countries, are reported. Recorded species distributions are listed by biogeographical region and by country. Microgastrine wasps are recorded from all continents except Antarctica; specimens can be found in all major terrestrial ecosystems, from 82°N to 55°S, and from sea level up to at least 4,500 m a.s.l. The Oriental (46) and Neotropical (43) regions have the largest number of genera recorded, whereas the Palaearctic region (28) is the least diverse. Currently, the highest species richness is in the Palearctic region (827), due to more historical study there, followed by the Neotropical (768) and Oriental (752) regions, which are expected to be the most species rich. Based on ratios of Lepidoptera and Microgastrinae species from several areas, the actual world diversity of Microgastrinae is expected to be between 30,000–50,000 species; although these ratios were mostly based on data from temperate areas and thus must be treated with caution, the single tropical area included had a similar ratio to the temperate ones. Almost 45,000 specimens of Microgastrinae from 67 different genera (83% of microgastrine genera) have complete or partial DNA barcode sequences deposited in the Barcode of Life Data System; the DNA barcodes represent 3,545 putative species or Barcode Index Numbers (BINs), as estimated from the molecular data. Information on the number of sequences and BINs per genus are detailed in the checklist. Microgastrinae hosts are here considered to be restricted to Eulepidoptera, i.e., most of the Lepidoptera except for the four most basal superfamilies (Micropterigoidea, Eriocranioidea, Hepialoidea and Nepticuloidea), with all previous literature records of other insect orders and those primitive Lepidoptera lineages being considered incorrect. The following nomenclatural acts are proposed: 1) Two genera are synonymyzed under Apanteles: Cecidobracon Kieffer & Jörgensen, 1910, new synonym and Holcapanteles Cameron, 1905, new synonym; 2) Nine lectotype designations are made for Alphomelon disputabile (Ashmead, 1900), Alphomelon nigriceps (Ashmead, 1900), Cotesia salebrosa (Marshall, 1885), Diolcogaster xanthaspis (Ashmead, 1900), Dolichogenidea ononidis (Marshall, 1889), Glyptapanteles acraeae (Wilkinson, 1932), Glyptapanteles guyanensis (Cameron, 1911), Glyptapanteles militaris (Walsh, 1861), and Pseudapanteles annulicornis Ashmead, 1900; 3) Three new replacement names are a) Diolcogaster aurangabadensis Fernandez-Triana, replacing Diolcogaster indicus (Rao & Chalikwar, 1970) [nec Diolcogaster indicus (Wilkinson, 1927)], b) Dolichogenidea incystatae Fernandez-Triana, replacing Dolichogenidea lobesia Liu & Chen, 2019 [nec Dolichogenidea lobesia Fagan-Jeffries & Austin, 2019], and c) Microplitis vitobiasi Fernandez-Triana, replacing Microplitis variicolor Tobias, 1964 [nec Microplitis varicolor Viereck, 1917]; 4) Three names amended are Apanteles irenecarrilloae Fernandez-Triana, 2014, Cotesia ayerzai (Brèthes, 1920), and Cotesia riverai (Porter, 1916); 5) Seven species have their status revised: Cotesia arctica (Thomson, 1895), Cotesia okamotoi (Watanabe, 1921), Cotesia ukrainica (Tobias, 1986), Dolichogenidea appellator (Telenga, 1949), Dolichogenidea murinanae (Capek & Zwölfer, 1957), Hypomicrogaster acarnas Nixon, 1965, and Nyereria nigricoxis (Wilkinson, 1932); 6) New combinations are given for 318 species: Alloplitis congensis, Alloplitis detractus, Apanteles asphondyliae, Apanteles braziliensis, Apanteles sulciscutis, Choeras aper, Choeras apollion, Choeras daphne, Choeras fomes, Choeras gerontius, Choeras helle, Choeras irates, Choeras libanius, Choeras longiterebrus, Choeras loretta, Choeras recusans, Choeras sordidus, Choeras stenoterga, Choeras superbus, Choeras sylleptae, Choeras vacillatrix, Choeras vacillatropsis, Choeras venilia, Cotesia asavari, Cotesia bactriana, Cotesia bambeytripla, Cotesia berberidis, Cotesia bhairavi, Cotesia biezankoi, Cotesia bifida, Cotesia caligophagus, Cotesia cheesmanae, Cotesia compressithorax, Cotesia delphinensis, Cotesia effrena, Cotesia euphobetri, Cotesia elaeodes, Cotesia endii, Cotesia euthaliae, Cotesia exelastisae, Cotesia hiberniae, Cotesia hyperion, Cotesia hypopygialis, Cotesia hypsipylae, Cotesia jujubae, Cotesia lesbiae, Cotesia levigaster, Cotesia lizeri, Cotesia malevola, Cotesia malshri, Cotesia menezesi, Cotesia muzaffarensis, Cotesia neptisis, Cotesia nycteus, Cotesia oeceticola, Cotesia oppidicola, Cotesia opsiphanis, Cotesia pachkuriae, Cotesia paludicolae, Cotesia parbhanii, Cotesia parvicornis, Cotesia pratapae, Cotesia prozorovi, Cotesia pterophoriphagus, Cotesia radiarytensis, Cotesia rangii, Cotesia riverai, Cotesia ruficoxis, Cotesia senegalensis, Cotesia seyali, Cotesia sphenarchi, Cotesia sphingivora, Cotesia transuta, Cotesia turkestanica, Diolcogaster abengouroui, Diolcogaster agama, Diolcogaster ambositrensis, Diolcogaster anandra, Diolcogaster annulata, Diolcogaster bambeyi, Diolcogaster bicolorina, Diolcogaster cariniger, Diolcogaster cincticornis, Diolcogaster cingulata, Diolcogaster coronata, Diolcogaster coxalis, Diolcogaster dipika, Diolcogaster earina, Diolcogaster epectina, Diolcogaster epectinopsis, Diolcogaster grangeri, Diolcogaster heterocera, Diolcogaster homocera, Diolcogaster indica, Diolcogaster insularis, Diolcogaster kivuana, Diolcogaster mediosulcata, Diolcogaster megaulax, Diolcogaster neglecta, Diolcogaster nigromacula, Diolcogaster palpicolor, Diolcogaster persimilis, Diolcogaster plecopterae, Diolcogaster plutocongoensis, Diolcogaster psilocnema, Diolcogaster rufithorax, Diolcogaster semirufa, Diolcogaster seyrigi, Diolcogaster subtorquata, Diolcogaster sulcata, Diolcogaster torquatiger, Diolcogaster tristiculus, Diolcogaster turneri, Diolcogaster vulcana, Diolcogaster wittei, Distatrix anthedon, Distatrix cerales, Distatrix cuspidalis, Distatrix euproctidis, Distatrix flava, Distatrix geometrivora, Distatrix maia, Distatrix tookei, Distatrix termina, Distatrix simulissima, Dolichogenidea agamedes, Dolichogenidea aluella, Dolichogenidea argiope, Dolichogenidea atreus, Dolichogenidea bakeri, Dolichogenidea basiflava, Dolichogenidea bersa, Dolichogenidea biplagae, Dolichogenidea bisulcata, Dolichogenidea catonix, Dolichogenidea chrysis, Dolichogenidea coffea, Dolichogenidea coretas, Dolichogenidea cyane, Dolichogenidea diaphantus, Dolichogenidea diparopsidis, Dolichogenidea dryas, Dolichogenidea earterus, Dolichogenidea ensiger, Dolichogenidea eros, Dolichogenidea evadne, Dolichogenidea falcator, Dolichogenidea gelechiidivoris, Dolichogenidea gobica, Dolichogenidea hyalinis, Dolichogenidea iriarte, Dolichogenidea lakhaensis, Dolichogenidea lampe, Dolichogenidea laspeyresiella, Dolichogenidea latistigma, Dolichogenidea lebene, Dolichogenidea lucidinervis, Dolichogenidea malacosomae, Dolichogenidea maro, Dolichogenidea mendosae, Dolichogenidea monticola, Dolichogenidea nigra, Dolichogenidea olivierellae, Dolichogenidea parallelis, Dolichogenidea pelopea, Dolichogenidea pelops, Dolichogenidea phaenna, Dolichogenidea pisenor, Dolichogenidea roepkei, Dolichogenidea scabra, Dolichogenidea statius, Dolichogenidea stenotelas, Dolichogenidea striata, Dolichogenidea wittei, Exoryza asotae, Exoryza belippicola, Exoryza hylas, Exoryza megagaster, Exoryza oryzae, Glyptapanteles aggestus, Glyptapanteles agynus, Glyptapanteles aithos, Glyptapanteles amenophis, Glyptapanteles antarctiae, Glyptapanteles anubis, Glyptapanteles arginae, Glyptapanteles argus, Glyptapanteles atylana, Glyptapanteles badgleyi, Glyptapanteles bataviensis, Glyptapanteles bistonis, Glyptapanteles borocerae, Glyptapanteles cacao, Glyptapanteles cadei, Glyptapanteles cinyras, Glyptapanteles eryphanidis, Glyptapanteles euproctisiphagus, Glyptapanteles eutelus, Glyptapanteles fabiae, Glyptapanteles fulvigaster, Glyptapanteles fuscinervis, Glyptapanteles gahinga, Glyptapanteles globatus, Glyptapanteles glyphodes, Glyptapanteles guierae, Glyptapanteles horus, Glyptapanteles intricatus, Glyptapanteles lamprosemae, Glyptapanteles lefevrei, Glyptapanteles leucotretae, Glyptapanteles lissopleurus, Glyptapanteles madecassus, Glyptapanteles marquesi, Glyptapanteles melanotus, Glyptapanteles melissus, Glyptapanteles merope, Glyptapanteles naromae, Glyptapanteles nepitae, Glyptapanteles nigrescens, Glyptapanteles ninus, Glyptapanteles nkuli, Glyptapanteles parasundanus, Glyptapanteles penelope, Glyptapanteles penthocratus, Glyptapanteles philippinensis, Glyptapanteles philocampus, Glyptapanteles phoebe, Glyptapanteles phytometraduplus, Glyptapanteles propylae, Glyptapanteles puera, Glyptapanteles seydeli, Glyptapanteles siderion, Glyptapanteles simus, Glyptapanteles speciosissimus, Glyptapanteles spilosomae, Glyptapanteles subpunctatus, Glyptapanteles thespis, Glyptapanteles thoseae, Glyptapanteles venustus, Glyptapanteles wilkinsoni, Hypomicrogaster samarshalli, Iconella cajani, Iconella detrectans, Iconella jason, Iconella lynceus, Iconella pyrene, Iconella tedanius, Illidops azamgarhensis, Illidops lamprosemae, Illidops trabea, Keylimepie striatus, Microplitis adisurae, Microplitis mexicanus, Neoclarkinella ariadne, Neoclarkinella curvinervus, Neoclarkinella sundana, Nyereria ituriensis, Nyereria nioro, Nyereria proagynus, Nyereria taoi, Nyereria vallatae, Parapanteles aethiopicus, Parapanteles alternatus, Parapanteles aso, Parapanteles atellae, Parapanteles bagicha, Parapanteles cleo, Parapanteles cyclorhaphus, Parapanteles demades, Parapanteles endymion, Parapanteles epiplemicidus, Parapanteles expulsus, Parapanteles fallax, Parapanteles folia, Parapanteles furax, Parapanteles hemitheae, Parapanteles hyposidrae, Parapanteles indicus, Parapanteles javensis, Parapanteles jhaverii, Parapanteles maculipalpis, Parapanteles maynei, Parapanteles neocajani, Parapanteles neohyblaeae, Parapanteles nydia, Parapanteles prosper, Parapanteles prosymna, Parapanteles punctatissimus, Parapanteles regalis, Parapanteles sarpedon, Parapanteles sartamus, Parapanteles scultena, Parapanteles transvaalensis, Parapanteles turri, Parapanteles xanthopholis, Pholetesor acutus, Pholetesor brevivalvatus, Pholetesor extentus, Pholetesor ingenuoides, Pholetesor kuwayamai, Promicrogaster apidanus, Promicrogaster briareus, Promicrogaster conopiae, Promicrogaster emesa, Promicrogaster grandicula, Promicrogaster orsedice, Promicrogaster repleta, Promicrogaster typhon, Sathon bekilyensis, Sathon flavofacialis, Sathon laurae, Sathon mikeno, Sathon ruandanus, Sathon rufotestaceus, Venanides astydamia, Venanides demeter, Venanides parmula, and Venanides symmysta.

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          DNA barcodes for ecology, evolution, and conservation.

          The use of DNA barcodes, which are short gene sequences taken from a standardized portion of the genome and used to identify species, is entering a new phase of application as more and more investigations employ these genetic markers to address questions relating to the ecology and evolution of natural systems. The suite of DNA barcode markers now applied to specific taxonomic groups of organisms are proving invaluable for understanding species boundaries, community ecology, functional trait evolution, trophic interactions, and the conservation of biodiversity. The application of next-generation sequencing (NGS) technology will greatly expand the versatility of DNA barcodes across the Tree of Life, habitats, and geographies as new methodologies are explored and developed.
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            THE POLYPHYLETIC NATURE OF APANTELES FOERSTER (HYMENOPTERA: BRACONIDAE): A PHYLOGENY AND RECLASSIFICATION OF MICROGASTRINAE

             W. Mason (1981)
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              Review of Apanteles sensu stricto (Hymenoptera, Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica

              Abstract 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.
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                Author and article information

                Journal
                ZooKeys
                ZK
                Pensoft Publishers
                1313-2970
                1313-2989
                March 23 2020
                March 23 2020
                : 920
                : 1-1089
                Article
                10.3897/zookeys.920.39128
                7197271
                32390740
                © 2020

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