Integrative taxonomy resuscitates two species in the Lasioglossum villosulum complex (Kirby, 1802) (Hymenoptera: Apoidea: Halictidae)

  • Alain Pauly Royal Belgian Institute of Natural Sciences, O.D. Taxonomy and Phylogeny & JEMU, rue Vautier 29, B-1000 Brussels
  • Grégoire Noël Functional and Evolutionary Entomology, University of Liège - Gembloux Agro-Bio Tech, Passage des Déportés 2, B-5030 Gembloux
  • Gontran Sonet Royal Belgian Institute of Natural Sciences, O.D. Taxonomy and Phylogeny & JEMU, rue Vautier 29, B-1000 Brussels
  • David G. Notton Department of Life Sciences, Insects Division, Darwin Centre - Room 315, The Natural History Museum, Cromwell Road, London, SW7 5BD
  • Jean-Luc Boevé Royal Belgian Institute of Natural Sciences, O.D. Taxonomy and Phylogeny & JEMU, rue Vautier 29, B-1000 Brussels
DOI: https://doi.org/10.5852/ejt.2019.541
Keywords: bees, Palaearctic, COI, phylogeny, morphology, integrative taxonomy, cryptic species

Abstract

Morphological and allozyme analyses suggested the occurrence of a pseudocryptic species in the Lasioglossum villosulum (Kirby, 1802) species complex (Hymenoptera: Halictidae). We analysed the morphology of more than 1500 specimens and the DNA barcode fragment of the cytochrome c oxidase subunit I (COI) of 102 specimens of this species complex from several Palaearctic countries. Our phylogenetic tree reconstructions, based on maximum likelihood and Bayesian inference revealed one clade corresponding to all specimens morphologically identified as Lasioglossum medinai (Vachal, 1895) and one divergent specimen morphologically identified as Lasioglossum berberum (Benoist, 1941). The other specimens, morphologically identified as L. villosulum, aggregated into at least three other lineages in our phylogenetic trees. The tree-based species delineations methods based on the Generalized Mixed Yule Coalescent (GMYC) model and the Bayesian Poisson Tree Process (bPTP) identified five to ten candidate species within the L. villosulum species complex, with L. medinai and L. berberum consistently recognized as separated from all other candidate species. Diagnostic morphological differences were found among L. medinai, L. berberum and the remaining specimens identified as L. villosulum. No diagnostic morphological differences were found to distinguish the different phylogenetic candidate species or lineages found within L. villosulum and L. medinai. Thus, both genetic and morphological approaches support the existence of L. medinai and L. berberum as distinct species from L. villosulum.

References

Amiet F., Herrmann M., Müller A. & Neumeyer R. 2001. Apidae 3. Halictus, Lasioglossum. Fauna Helvetica 3, Centre suisse de Cartographie de la Faune, Neuchâtel.

Azuma S. & Kinjo M. 1987. Checklist of the Insects of Okinawa. Flora and fauna in Okinawa 1, University Ryukyus Nishihara, Okinawa.

Benoist R. 1941. Récoltes de R. Paulian et A. Villiers dans le Haut Atlas Marocain, 1938 (18. Note). Hyménoptères Apidés. Annales de la Société entomologique de France 110: 79–82.

Blüthgen P. 1920. Die deutschen Arten der Bienengattung Halictus Latr. (Hym.). Deutsche Entomo-logische Zeitschrift 1920: 81–302.

Blüthgen P. 1922. Beiträge zur Synonymie der Bienengattung Halictus Latr. Deutsche Entomologische Zeitschrift 1922: 46–66, 316–321.

Blüthgen P. 1923. Beiträge zur Synonymie der Bienengattung Halictus Latr. III. Deutsche Entomo-logische Zeitschrift 1923: 239–242.

Blüthgen P. 1926. Beiträge zur Kenntnis der indo-malayischen Halictus und Thrincostoma Arten (Hym. Apidae, Halictini). Zoologische Jahrbucher Jena (Systematik, Geographie und Biologie der Tiere) 51: 375–698.

Blüthgen P. 1928. Beiträge zur Kenntnis der indo-malayischen Halictus und Thrincostoma - Arten. 1 Nachtrag. Zoologische Jahrbucher Jena (Systematik, Geographie und Biologie der Tiere) 54: 343–406.

Blüthgen P. 1930. Halictus Latr. In: Schmiedeknecht O. (ed.) Die Hymenopteren Nord- und Mittel-europas: 729–767. Fischer Verlag, Jena.

Blüthgen P. 1933. Ein Beitrag zur Kenntnis der Bienenfauna Aegyptens (Hymenoptera: Apidae-Halictidae-Halictinae). Bulletin de la Société royale entomologique d’Egypte 1933 (1–3): 14–27.

Bossert S., Gereben-Krenn B.-A., Neumayer J., Schneller B. & Krenn H.W. 2016. The cryptic Bombus lucorum complex (Hymenoptera: Apidae) in Austria: phylogeny, distribution, habitat usage and a climatic characterization based on COI sequence data. Zoological Studies 55 (13): 1–15. https://doi.org/10.6620/ZS.2016.55-13

Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C-H., Xie D., Suchard M.A., Rambaut A. & Drummond A.J. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10 (4): e1003537. https://doi.org/10.1371/journal.pcbi.1003537

Bytinsky-Salz H. & Ebmer A.W. 1974. The Halictidae of Israel (Hymenoptera, Apoidea). II. Genus Lasioglossum. Israel Journal of Entomology 9: 175–217.

Cockerell T.D.A. 1938a. Descriptions and Records of Bees - CLXVI. Annals and Magazine of Natural History Series 11.1 (1): 79–85. https://doi.org/10.1080/00222933808526744

Cockerell T.D.A 1938b. Halictine bees from Morocco. American Museum Novitates 997: 1–9.

Dalla Torre C.G. de 1896. Catalogus Hymenopterorum hucusque descriptorum systematicus et synonymicus. Vol X. Apidae (Anthophila). Engelmann, Leipzig.

Danforth B.N. 1999. Phylogeny of the bee genus Lasioglossum (Hymenoptera: Halictidae) based on mitochondrial COI sequence data. Systematic Entomology 24 (4): 377–393. https://doi.org/10.1046/j.1365-3113.1999.00087.x

Danforth B.N. 2002. Evolution of sociality in a primitively eusocial lineage of bees. Proceedings of the National Academy of Sciences 99 (1): 286–290.

Dathe H.H. 2009. Order Hymenoptera, superfamily Apoidea. Families Colletidae, Andrenidae, Halictidae, Melittidae, Megachilidae and Apidae. Arthropod Fauna of the UAE 2: 335–432.

Ebmer A.W. 1974. Beiträge zur Kenntnis der Fauna Afghanistans. Halictus Latr. et Lasioglossum Curt., Halictidae, Apoidea, Hymenoptera. Časopis Moravského musea v Brně 59: 183–210.

Ebmer A.W. 1975. Die Typen und Typoide des Natur-Museum Senckenberg 54 Von Schenck beschriebene Halictidae (Ins.: Hymenoptera: Apoidea). Senckenbergiana Biologica 56: 233–246.

Ebmer A.W. 1976. Halictus and Lasioglossum aus Marokko. Linzer biologische Beiträge 8 (1): 205–288.

Ebmer A.W. 1978a. Die Halictidae der Mandschurei (Apoidea, Hymenoptera). Bonner Zoologische Beiträge 29: 183–221.

Ebmer A.W. 1978b. Die Bienen der Gattungen Halictus Latr., Lasioglossum Curt. und Dufourea Lep. (Hymenoptera, Halictidae) aus Korea. Annales Historico-Naturales Musei Nationalis Hungarici 70: 307–319.

Ebmer A.W. 1978c. Halictus, Lasioglossum, Rophites und Systropha aus dem Iran. Linzer biologische Beiträge 10: 1–109.

Ebmer A.W. 1982. Zur Bienenfauna der Mongolei. Die Arten der Gattungen Halictus Latr. und Lasioglossum Curt. (Hymenoptera: Halictidae). Ergebnisse der Mongolisch-Deutschen Biologischen Expedition seit 1962, Nr 108. Mitteilungen aus dem Zoologischen Museum in Berlin 58(2): 199–227.

Ebmer A.W. 1988. Kritische Liste der nicht-parasitischen Halictidae Österreichs mit Berücksichtigung aller mitteleuropaïschen Arten (Insecta: Hymenoptera: Apoidea: Halictidae). Linzer biologische Beiträge 20 (2): 527–711.

Ebmer A.W. 1996. Asiatische Halictidae, 5. Daten zur Aculeaten-Fauna der Ussuri-Region unter Berücksichtigung der angrenzenden Gebiete (Insecta: Hymenoptera: Apoidea: Halictidae: Halictinae). Linzer biologische Beiträge 28 (1): 261–304.

Ebmer A.W. 2004. Zur Bienenfauna Nepals: Arten der Gattungen Halictus, Lasioglossum und Dufourea (Insecta: Hymenoptera: Apoidea: Halictidae). Veröffentichungen Naturmuseum Erfurt 23: 123–150.

Ebmer A.W. 2005. Zur Bienenfauna der Mongolei. Die Arten der Gattungen Halictus Latr. und Lasioglossum Curt. (Insecta: Hymenoptera: Apoidea: Halictidae: Halictinae), Ergänzungen und Korrekturen. Linzer biologische Beiträge 37 (1): 343–392.

Ebmer A.W. 2006. Daten zur Aculeaten-Fauna der Ussuri-Region unter Berücksichtigung der angrenzenden Gebiete - 2 Arten der Gattungen Halictus, Lasioglossum, Dufourea, Macropis aus dem Lazovski Zapovednik - Naturrervat Laso (Insecta: Hymenoptera: Apoidea: Halictidae, Melittidae). Linzer biologische Beiträge 38 (1): 541–593.

Ebmer A.W. 2008. Neue Taxa der Gattungen Halictus Latreille 1804 und Lasioglossum Curtis 1833 (Hymenoptera, Apoidea, Halictidae) aus den Vereinigten Arabischen Emiraten. Linzer biologische Beiträge 40 (1): 551–580.

Ezard T., Fujisawa T. & Barraclough T.G. 2017. splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-19/r52. Available from https://R-Forge.R-project.org/projects/splits/ [accessed 8 Jun. 2019].

Fellendorf M., Mohra C., Roberts S., Wirtz P. & van der Zanden G. 1999. The bees of Madeira (Hymenoptera, Apoidea). Bocagiana, Museu Municipal do Funchal (Historia Natural) 197: 1–17.

Ferrari R.R. 2019. A revision of Colletes Latreille (Hymenoptera: Colletidae: Colletinae) from Brazil, Paraguay and Uruguay. Zootaxa 4606 (1): 1–91. https://doi.org/10.11646/zootaxa.4606.1.1

Folmer O., Black M., Hoe W., Lutz R. & Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3 (5): 294–299.

Françoso E. & Arias M.C. 2013. Cytochrome c oxidase I primers for corbiculate bees: DNA barcode and mini-barcode. Molecular Ecology 13: 844–850. https://doi.org/10.1111/1755-0998.12135

Fujisawa T. & Barraclough T.G. 2013. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62: 707–724. https://doi.org/10.1093/sysbio/syt033

Gibbs J. 2018. DNA barcoding a nightmare taxon: assessing barcode index numbers and barcode gaps for sweat bees. Genome 61 (1): 21–31. https://doi.org/10.1139/gen-2017-0096

Gibbs J., Brady S.G., Kanda K. & Danforth B.N. 2012. Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Molecular Phylogenetics and Evolution 65 (3): 926–939. https://doi.org/10.1016/j.ympev.2012.08.013

Gibbs J., Packer L., Dumesh S. & Danforth B. 2013. Revision and reclassification of Lasioglossum (Evylaeus), L. (Hemihalictus) and L. (Sphecodogastra) in Eastern North America (Hymenoptera, Apoidea, Halictidae). Zootaxa 3672: 1–117. https://doi.org/10.11646/zootaxa.3672.1.1

Goaga A. 2003. Contributii la studiul specilior de Halictide (Apoidea: Halictidae) din Fauna Moldavei. Complexul Muzeal de Ştiinţele Naturii “Ion Borcea” Bacău, Studii şi Comunicări 2000–2003: 181–195.

Gogala A. 1999. Bee fauna of Slovenia: checklist of species (Hymenoptera Apoidea). Scopolia 42: 1–79.

Gonzáles-Vaquero R.A. & Roig-Alsina A. 2019. The bee Ruizanthedella mutabilis Spinola (Hymenoptera: Halictidae): a very common but poorly known species studied using integrative taxonomy. Zootaxa 4563 (1): 191–200. https://doi.org/10.11646/zootaxa.4563.1.12

González-Vaquero R.A., Roig-Alsina A. & Packer L. 2016. DNA barcoding as a useful tool in the systematic study of wild bees of the tribe Augochlorini (Hymenoptera: Halictidae). Genome 59: 889–898. https://doi.org/10.1139/gen-2016-0006

Haneda Y. 1990. [On the Apoidea (Hymenoptera) of Fukui Prefecture, Japan (4)]. Entomological Journal of Fukui 7: 2–10. [In Japanese.]

Hebert P.D.N., Ratnasingham S., Zakharov E.V., Telfer A.C., Levesque-Beaudin V., Milton M.A., Pedersen S., Jannetta P. & de Waard J.R. 2016. Counting animal species with DNA barcodes: Canadian insects. Philosophical Transactions of the Royal Society of London B 371: 20150333. https://doi.org/10.1098/rstb.2015.0333

Hillis D. & Bull J.J. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42 (2): 182–192.

Huelsenbeck J.P. & Rannala B. 2004. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53 (6): 904–913.

Kirby W. 1802. Monographia Apum Angliae. Vols 1–2. Privately published, Ipswich.

Kress W.J., Garcia-Robledo C., Uriarte M. & Erickson D.L. 2015. DNA barcodes for ecology, evolution, and conservation. Trends in Ecology & Evolution 30 (1): 25–35. https://doi.org/10.1016/j.tree.2014.10.008

Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Evolutionary Genetics Analysis 33 (7): 1870–1874. https://doi.org/10.1093/molbev/msw054

Lajus D., Sukhikh N. & Alekseev V. 2015. Cryptic or pseudocryptic: can morphological methods inform copepod taxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex. Ecology and Evolution 5 (12): 2374–2385. https://doi.org/10.1002/ece3.1521

Landaverde-González P., Moo-Valle H., Murray T.E., Paxton R.J., Quezada-Euan J.J.G. & Husemann M. 2017. Sympatric lineage divergence in cryptic Neotropical sweat bees (Hymenoptera: Halictidae: Lasioglossum). Organisms Diversity & Evolution 17: 251–265. https://doi.org/10.1007/s13127-016-0307-1

Lanfear R., Calcott B., Ho S.Y. & Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29 (6): 1695–1701. https://doi.org/10.1093/molbev/mss020

Lanfear R., Frandsen P.B., Wright A.M., Senfeld T. & Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34 (3): 772–773. https://doi.org/10.1093/molbev/msw260

Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGerrigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thomson J.D., Gibson T.J. & Higgins D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23 (1): 2947–2948. https://doi.org/10.1093/bioinformatics/btm404

Levchenko T.V. 2015. Contributions to the fauna of bees (Hymenoptera: Apoidea) of Moscow Province. 5. Family Halictidae. Genera Lasioglossum Curtis, 1833 and Evylaeus Robertson, 1902. Eversmannia 43–44: 20–43.

Luo A., Ling C., Ho S.Y.W & Zhu C.D. 2018. Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67: 830–846. https://doi.org/10.1093/sysbio/syy011

Magnacca K.N. & Brown M.J. 2012. Barcoding a regional fauna: Irish solitary bees. Molecular Ecology Research 12: 990–998. https://doi.org/10.1111/1755-0998.12001

Michonneau F. 2016. Using GMYC for Species Delination. Available from https://zenodo.org/record/838260#.XPuNfi-B3Vo [accessed 25 March 2019].

Michonneau F., Bolker B., Holder M., Lewis P. & O’Meara B. 2018. rncl: An Interface to the Nexus Class Library. R package version 0.8.3. Available from https://CRAN.R-project.org/package=rncl [accessed 8 Jun. 2019].

Murao R. 2017. Bees of the Hemihalictus series of Lasioglossum Curtis (Hymenoptera, Halictidae) in South Korea. Zootaxa 4268 (4): 451–488. https://doi.org/10.11646/zootaxa.4268.4.1

Natural History Museum. 2014. Dataset: Collection specimens. Resource: Specimens. Natural History Museum Data Portal. https://doi.org/10.5519/0002965 [accessed 25 Nov. 2018].

Ortiz-Sánchez F.J. & Pauly A. 2017. Contribution à la connaissance des Halictinae d’Espagne, avec un atlas des espèces de la Péninsule Ibérique (Hymenoptera: Apoidea: Halictidae). Belgian Journal of Entomology 54: 1–92.

Packer L., Porsa A., Plateaux-Quénu C. & Plateaux L. 1999. A cryptic species allied to Evylaeus villosulus (Kirby) (Hymenoptera: Halictidae). Annales de la Société entomologique de France (N.S.) 35 (2): 165–171.

Padial J.M., Miralles A., De la Riva I. & Vences M. 2010. The integrative future of taxonomy. Frontiers in Zoology 7 (1): 1–14. https://doi.org/10.1186/1742-9994-7-16

Paradis E. 2010. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26: 419–420.

Paradis E. & Schliep K. 2018. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 (1): 526–528. https://doi.org/10.1093/bioinformatics/bty633

Pauly A. & Belval S. 2017. Atlas des Halictidae de France (Hymenoptera: Apoidea). Belgian Journal of Entomology 53: 1–34.

Pauly A., Devalez J., Sonet G., Nagy Z.T. & Boevé J.-L. 2015. DNA barcoding and male genital morphology reveal five new cryptic species in the West Palaearctic bee Seladonia smaragdula (Vachal, 1895) (Hymenoptera: Apoidea: Halictidae). Zootaxa 4034 (2): 257–290. https://doi.org/10.11646/zootaxa.4034.2.2

Pentinsaari M., Vos R. & Mutanen M. 2017. Algorithmic single-locus species delimitation: effects of sampling effort, variation and nonmonophyly in four methods and 1870 species of beetles. Molecular Ecology Resources 17: 393–404. https://doi.org/10.1111/1755-0998.12557

Pesenko Y.A. 2007a. Subgeneric classification of the Palaearctic bees of the genus Evylaeus Robertson (Hymenoptera: Halictidae). Zootaxa 1500: 1–54.

Pesenko Y.A. 2007b. A taxonomic study of the bee genus Evylaeus Robertson of Eastern Siberia and the Far East of Russia (Hymenoptera: Halictidae). Zoosystematica Rossica 16: 79–123.

Pesenko Y., Banaszak J., Radchenko V. & Cierzniak T., 2000. Bees of the Family Halictidae (excluding Sphecodes) of Poland: Taxonomy, Ecology, Bionomics. University Publishers of the Pedagogical School, Bydgoszcz, Poland.

Plateaux-Quénu C. 1993. Modalités de la socialisation chez les Halictinae (Hymenoptera, Halictidae). I. Biologie des Halictinae. Année biologique 32 (4): 183–204.

Plateaux-Quénu C. & Plateaux L. 1981. La variation individuelle d’Evylaeus villosulus (K.), espèce solitaire (Hym. Halictinae). I. Fondatrices de printemps. Annales des Sciences naturelles, Zoologie 13e Série 3: 249–258.

Plateaux-Quénu C. & Plateaux L. 1985. La variation individuelle d’Evylaeus villosulus (K.), espèce solitaire (Hym., Halictinae). Comparaison des fondatrices de printemps et de leurs filles, appartenant à la première génération. Actes des Colloques Insectes sociaux 2: 293–302.

Plateaux-Quénu C. & Plateaux L. 1986. Alternance de générations chez Evylaeus villosulus (K.) (Hym. Halictinae). Actes Colloques internationaux U.I.E.I.S., section française 1985 3: 73–82.

Plateaux-Quénu C. & Plateaux L. 1987. Présence de fondatrices géantes dans deux populations d’Evylaeus villosulus (K.) (Hym., Halictinae). Annales des Sciences naturelles, Zoologie 13e série, 1986–1987 8: 259–266.

Plateaux-Quénu C. & Plateaux L. 1993. Dimorphisme des femelles dans une population d’Evylaeus villosulus (Kirby) (Hym., Halictinae). Bulletin de la Société zoologique de France 118 (4): 387–393.

Plateaux-Quénu C., Plateaux L. & Packer L. 1987. Preadaptations to sociality in the solitary, bivoltine Halictine bee Evylaeus villosulus (K.). Evolution of Insects Societies. Chemistry and Biology of Social Insects. J. Peperny, Munich.

Plateaux-Quénu C., Plateaux L. & Packer L. 1989. Biological notes on Evylaeus villosulus (K.) (Hymenoptera, Halictidae), a bivoltine, largely solitary halictine bee. Insectes sociaux, Paris 36 (4): 245–263.

Pridal A. 2004. Checklist of the bees in the Czech Republic and Slovakia with comments on their distribution and taxonomy (Insecta: Hymenoptera: Apoidea). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 52: 29–65.

Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P., Hazell S., Kamoun S., Sumlin W.D. & Vogler A.P. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 1–15. https://doi.org/10.1080/10635150600852011

Praz C., Müller A. & Genoud D. 2019. Hidden diversity in European bees: Andrena amieti sp. n., a new Alpine bee species related to Andrena bicolor (Fabricius, 1775) (Hymenoptera, Apoidea, Andrenidae). Alpine Entomology 3: 11–38. https://doi.org/10.3897/alpento.3.29675

Rambaut A. 2017. Figtree 1.4.0. Available from http://tree.bio.ed.ac.uk/software/figtree/ [accessed 18 Aug. 2017].

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032

Rasmussen C., Schmidt H.T. & Madsen H.B. 2016. Distribution, phenology and host plants of Danish bees (Hymenoptera, Apoidea). Zootaxa 4212 (1): 1–100. https://doi.org/10.11646/zootaxa.4212.1.1

Ratnasingham S. & Hebert P.D.N. 2013. A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8 (7): e66213. https://doi.org/10.1371/journal.pone.0066213

Ronquist F., Teslenko M., van der Mark P., Darling A., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029

Schenck A. 1869. Beschreibung der nassauischen Bienen. II. Nachtrag. Jahrbücher des Nassauischen Vereins für Naturkunde 21–22 (1867–1868): 301–312 (Halictus), 375 (Nachträge).

Schmidt S., Schmid-Egger C., Morinière J., Haszprunar G. & Hebert P.D.N. 2015. DNA barcoding largely supports 250 years of classical taxonomy: identifications for Central European bees (Hymenoptera, Apoidea partim). Molecular Ecology Resources 15 (4): 985–1000. https://doi.org/10.1111/1755-0998.12363

Simon C., Frati F., Beckenbach A., Crespi B., Hong Liu & Flook P. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87 (6): 651–701.

Strand E. 1909. Die paläarktischen Halictus-Arten des Kgl. Zoologischen Museums zu Berlin, z.T. nach Bestimmungen von J. D. Alfken. Archiv für Naturgeschichte 75 I (1): 1–62.

Strand E. 1914. H. Sauter Formosa Ausbeute: Apidae II (Die Halictus-Arten von Formosa). Archiv für Naturgeschichte A 12 (1913): 147–171.

Struck T.H., Feder J.L., Bendiksby M., Birkeland S., Cerca J., Gusarov V.I., Kistenich S., Larrson K.- H., Lee Hsiang Liow, Nowak M.D., Stedje B., Bachmann L. & Dimitrov D. 2017. Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution: 1–11. https://doi.org/10.1016/j.tree.2017.11.007

Sukumaran J. & Holder M.T. 2010. DendroPy: a Python library for phylogenetic computing. Bioinfor-matics 26: 1569–1571. https://doi.org/10.1093/bioinformatics/btq228

Sukumaran J. & Holder M.T. 2017. SumTrees: Phylogenetic Tree Summarization. Ver. 4.3.0. Available from https://github.com/jeetsukumaran/DendroPy [accessed 16 Feb 2018].

Svensson B.G., Erlandsson S. & Janzon L.-A. 1990. Catalogus Insectorum Sueciae. Hymenoptera, Apoidea. 2. Andrenidae and Halictidae. Entomologisk Tidskrift 111: 47–52.

Takahashi H. & Sakagami S.F. 1993. Notes on the halictine bees (Hymenoptera Apoidea) of the Izu Islands: Lasioglossum kuroshio sp. nov., life cycles in Hachijo-jima Is., and a preliminary list of the species in the Izu Islands. Japanese Journal of Entomology 61 (2): 267–278.

Tang C.Q., Humphreys A.M., Fontaneto D., Barraclough T.G. 2014. Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data. Methods in Ecology and Evolution 5 (10): 1086–1094. https://doi.org/10.1111/2041-210X.12246

Tang C.Q., Notton D.G., Norman H. & Vogler A. 2018. Taxonomic Fellowship to Support the National Pollinators Strategy - EVID4 Evidence Project Final Report. Department for Environment, Food and Rural Affairs and The Natural History Museum, London.

Usui M., Nishijuma Y., Fukuda H. & Sakagami S.F. 1976. A wild bee survey in Obihiro, eastern Hokkaido. Research Bulletin of Obihiro University 10: 225–251.

Vachal J. 1895. Halictus nouveaux de la collection Medina. Anales de la Sociedad Española de Historia Natural 24: 147–150.

Warncke K. 1973. Zur Systematik und Synonymie der mitteleuropäischen Furchenbienen Halictus Latreille (Hymenoptera, Apoidea, Halictidae). Bulletin de la Société royale des Sciences de Liège 42 (7–8): 277–295.

Warncke K. 1975a. Beitrag zur Systematik und Verbreitung der Furchenbienen in der Türkei (Hymenoptera, Apoidea, Halictus). Polskie Pismo Entomologiczne 45: 81–128.

Warncke K. 1975b. Zur Kenntnis der Bienengattung Halictus Latr. auf den Kanarischen Inseln (Hym., Apoidea). Vieraea 4: 201–223.

Warncke K. 1976. Bemerkungen zu der Arbeit von Ebmer über die als Apis beschriebenen Bienen der Gattung Halictus und ein Beitrag zur Namensklärung nordafrikanischer Bienen der gleichen Gattung (Hym. Apidae). Nachrichtenblatt der Bayerischen Entomologen 25 (5): 89–96.

Weissmann J.A., Picanço A., Borges P.A.V. & Schaefer H. 2017. Bees of the Azores: an annotated checklist (Apidae, Hymenoptera). Zookeys 642: 63–95. https://doi.org/10.3897/zookeys.642.10773

Wilcox T.P., Zwickl D.J., Heath T.A. & Hillis D.M. 2002. Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution 25: 361–371. https://doi.org/10.1016/S1055-7903(02)00244-0

Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 (22): 2869–2876. https://doi.org/10.1093/bioinformatics/btt499

Zwickl D.J. 2006. Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion. Ph.D. dissertation, The University of Texas at Austin. Available from http://hdl.handle.net/2152/2666 [accessed 4 Jul. 2019].

Published
2019-08-01
How to Cite
Pauly, A., Noël, G., Sonet, G., Notton, D. G., & Boevé, J.-L. (2019). Integrative taxonomy resuscitates two species in the Lasioglossum villosulum complex (Kirby, 1802) (Hymenoptera: Apoidea: Halictidae). European Journal of Taxonomy, (541). https://doi.org/10.5852/ejt.2019.541
Issue
No. 541 (2019): Integrative taxonomy resuscitates two species in the Lasioglossum villosulum complex (Kirby, 1802) (Hymenoptera: Apoidea: Halictidae)
Section
Entomology

Copyright (c) 2019 Alain Pauly, Grégoire Noël, Gontran Sonet, David G. Notton, Jean-Luc Boevé

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Creative Commons Copyright Notices

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are NOT PERMITTED to post their submitted work online (e.g., in institutional repositories or on personal websites) prior to publication, as it may lead to nomenclatural issues.