Revision of the Nearctic species of the Lasioglossum (Dialictus) gemmatum species complex (Hymenoptera: Halictidae)

Keywords: Apoidea, new species, phylogeny, taxonomy, tegula

Abstract

The Lasioglossum (Dialictus) gemmatum species complex, also known as the L. tegulare species group and the L. parvum species complex, is a very common, widespread, diverse, and recognisable lineage of sweat bees, containing 22 previously described species and several known undescribed species. The species were recently revised for the eastern Nearctic region and the Greater Antilles, but remain poorly known in the western Nearctic along with most other L. (Dialictus). These characteristics make it a prime candidate for revision in ongoing taxonomic work on the western Nearctic L. (Dialictus). Here we present the results of this revision, including 10 new species descriptions, one new synonymy, a preliminary phylogeny, and keys to known Nearctic species. Species of the eastern Nearctic and a few primarily Neotropical species which can occur in the Nearctic are also included. We report that the L. (D.) gemmatum species complex is likely a monophyletic group arising from the L. (D.) comulum group, but that the enlarged tegula has arisen independently in at least two other L. (Dialictus) lineages, and it contains multiple cases of allopatric speciation. The following species are described as new: Lasioglossum (Dialictus) angelicum sp. nov., L. (D.) deludens sp. nov., L. (D.) diabolicum sp. nov., L. (D.eremum sp. nov., L. (D.) gloriosum sp. nov., L. (D.) indagator sp. nov., L. (D.) holzenthali sp. nov., L. (D.) magnitegula sp. nov., L. (D.) profundum sp. nov., and L. (D.) rufodeludens sp. nov. Previously undescribed males of L. (D.) perparvum (Ellis, 1914) and L. (D.) pseudotegulare (Cockerell, 1896) and the female of L. (D.) gaudiale (Sandhouse, 1924) are diagnosed and figured for the first time. Lasioglossum (Dialictus) hunteri (Crawford, 1932) is a new subjective junior synonym of L. (D.) ellisiae (Sandhouse, 1924). Pre-2022 specimen records of L. (D.) hunteri and L. (D.) tegulariforme (Crawford, 1907) are attributable to a heterogeneous mix of species, and records of L. (D.) perparvum are likely attributable to L. (D.) deludens.

References

Brown S.D.J., Collins R.A., Boyer S., Lefort M.C., Malumbres‐Olarte J., Vink C.J. & Cruickshank R.H. 2012. SPIDER: an R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources 12 (3): 562–565. https://doi.org/10.1111/j.1755-0998.2011.03108.x

Campbell J.W., Hanula J.L. & Waldrop T.A. 2007. Effects of prescribed fire and fire surrogates on floral visiting insects of the blue ridge province in North Carolina. Biological Conservation 134: 393–404. https://doi.org/10.1016/j.biocon.2006.08.029

Cane J.H. 1987. Estimation of bee size using intertegular span (Apoidea). Journal of the Kansas Entomological Society 60 (1): 145–147.

Cockerell T.D.A. 1896. Contributions from the New Mexico Biological Station.—I. Descriptions of new bees collected by Prof. C. H. T. Townsend in the state of Vera Cruz. The Annals and Magazine of Natural History; Zoology, Botany, and Geology 18 (106): 282–295. https://doi.org/10.1080/00222939608680457

Cockerell T.D.A. 1898. On some small bees from Arizona. The Canadian Entomologist 30 (9): 237–239. https://doi.org/10.4039/Ent30237-9

Cockerell T.D.A. 1899. Catálogo de las abejas de México. Oficina Tipografía de la Secretaría de Fomento, Mexico City, State of Mexico. https://doi.org/10.5962/bhl.title.60192

Cockerell T.D.A. 1916. Sunflower insects in California and South Africa. The Canadian Entomologist 48 (3): 76–79. https://doi.org/10.4039/Ent4876-3

Cockerell T.D.A. 1937. Bees from San Miguel Island, California. The Pan-Pacific Entomologist 13 (4): 148–157.

Corbin L.A.-J., Awde D.N. & Richards M.H. 2021. Phenological and social characterization of three Lasioglossum (Dialictus) species inferred from long-term trapping collections. Journal of Hymenoptera Research 88: 17–38. https://doi.org/10.3897/jhr.88.73220

Crane S. 2013. DNA extraction from museum insect specimens. Available from https://doi.org/10.6084/m9.figshare.741214.v4 [accessed 22 Oct. 2020].

Crawford J.C. 1907. New Halictinae from the western United States. Invertebrata Pacifica 1: 190–197.

Crawford J.C. 1932. New North American bees. Proceedings of the Entomological Society of Washington 34 (5): 69–78.

Creedy T.J., Norman H., Tang C.Q., Qing Chin K., Andujar C., Arribas P., O’Connor R.S., Carvell C., Notton D.G. & Vogler A.P. 2020. A validated workflow for rapid taxonomic assignment and monitoring of a national fauna of bees (Apiformes) using high throughput DNA barcoding. Molecular Ecology Resources 20 (1): 40–53. https://doi.org/10.1111/1755-0998.13056

Cresson E.T. 1872. Hymenoptera Texana. Transactions of the American Entomological Society 4: 153–292. https://doi.org/10.2307/25076272

Cresson E.T. 1887. Synopsis of the families and genera of the Hymenoptera of America, north of Mexico, together with a catalogue of the described species, and bibliography. Transactions of the American Entomological Society, Supplementary volume: i–vi, 1–350. https://doi.org/10.5962/bhl.title.5531

Cresson E.T. 1916. The Cresson types of Hymenoptera. Memoirs of the American Entomological Society 1: 1–141.

Cresson E.T. 1928. The types of Hymenoptera in the Academy of Natural Sciences of Philadelphia other than those of Ezra T. Cresson. Memoirs of the American Entomological Society 5: 1–90.

Dalla Torre C.G. 1896. Catalogus Hymenoptorum: Apidae (Anthophila). Sumptibus Guilelmi Engelmann, Leipzig.

De Luca P.A., Buchmann S.L., Galen C., Mason A.C. & Vallejo‐Marín M. 2019. Does body size predict the buzz‐pollination frequencies used by bees? Ecology and Evolution 9 (8): 4875–4887. https://doi.org/10.1002/ece3.5092

DeSalle R., Egan M.G. & Siddall M. 2005. The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 360 (1462): 1905–1916. https://doi.org/10.1098/rstb.2005.1722

Dibble A.C., Drummond F.A., Stubbs C., Veit M. & Ascher J.S. 2017. Bees of Maine, with a state species checklist. Northeastern Naturalist 24 (m15): 1–48. https://doi.org/10.1656/045.024.m1503

Donovall L.R. & vanEngelsdorp D. 2010. A checklist of the bees (Hymenoptera: Apoidea) of Pennsylvania. Journal of the Kansas Entomological Society 83 (1): 7–24. https://doi.org/10.2317/JKES808.29.1

Eickwort G.C. 1988. Distribution patterns and biology of West Indian sweat bees (Hymenoptera: Halictidae). In: Liebherr J.K. (ed.) Zoogeography of Caribbean Insects: 231–252. Cornell University Press, Ithaca, New York. https://doi.org/10.7591/9781501746017-012

Ellis M.D. 1914. New American bees of the genus Halictus (Hym.). Entomological News, and Proceedings of the Entomological Section of the Academy of Natural Sciences of Philadelphia 25 (3): 97–104.

Engel M.S. 2000. A new Lasioglossum from the Juan Fernandez Islands (Hymenoptera: Halictidae). Revista Chilena de Entomologia 27: 5–10.

FAO/UNESCO. 2007. Digital Soil Map of the World. ver. 3.6. FAO, Rome.

Fick S.E. & Hijmans R.J. 2017. WorldClim 2: new 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37 (12): 4302–4315. https://doi.org/10.1002/joc.5086

Fischer H. & Ebert E. 1999. Tegula function during free locust flight in relation to motor pattern, flight speed, and aerodynamic output. Journal of Experimental Biology 202 (6): 711–721. https://doi.org/10.1242/jeb.202.6.711

Folmer O., Black M., Hoeh 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 Resources 13: 844–850. https://doi.org/10.1111/1755-0998.12135

Gardner J.D. & Gibbs J. 2020. The ‘red-tailed’ Lasioglossum (Dialictus) (Hymenoptera: Halictidae) of the western Nearctic. European Journal of Taxonomy 725: 1–242. https://doi.org/10.5852/ejt.2020.725.1167

Gardner J.D. & Gibbs J. 2022. New and little-known Canadian Lasioglossum (Dialictus) (Hymenoptera: Halictidae) and an emended key to species. The Canadian Entomologist 154: 1–37. https://doi.org/10.4039/tce.2021.47

Gibbs J. 2009a. Integrative taxonomy identifies new (and old) species in the Lasioglossum (Dialictus) tegulare (Robertson) species group (Hymenoptera, Halictidae). Zootaxa 2032 (1): 1–38. https://doi.org/10.11646/zootaxa.2032.1.1

Gibbs J. 2009b. New species in the Lasioglossum petrellum species group identified through an integrative taxonomic approach. The Canadian Entomologist 141: 371–396. https://doi.org/10.4039/n09-020

Gibbs J. 2010. Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa 2591 (1): 1–382. https://doi.org/10.11646/zootaxa.2591.1.1

Gibbs J. 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 3073 (1): 1–216. https://doi.org/10.11646/zootaxa.3073.1.1

Gibbs J. 2018a. 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. 2018b. Bees of the genus Lasioglossum (Hymenoptera: Halictidae) from Greater Puerto Rico, West Indies. European Journal of Taxonomy 400: 1–57. https://doi.org/10.5852/ejt.2018.400

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: 926–939. https://doi.org/10.1016/j.ympev.2012.08.013

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

Grab H., Branstetter M.G., Amon N., Urban-Mead K.R., Park M.G., Gibbs J., Blitzer E.J., Poveda K., Loeb G. & Danforth B.N. 2019. Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services. Science 363 (6424): 282–284. https://doi.org/10.1126/science.aat6016

Graenicher S. 1927. Bees of the genus Halictus from Miami, Florida. Psyche 34: 203–208. https://doi.org/10.1155/1927/75420

Harris R.A. 1979. Glossary of surface sculpturing. Occasional Papers in Entomology 28: 1–31.

Hurd P.D. 1979. Superfamily Apoidea. In: Krombein K.V., Hurd P.D., Smith D.R. & Burks B.D. (eds) Catalog of Hymenoptera in America North of Mexico: 1741–2209. Smithsonian Institution Press, Washington, D.C.

ICZN. 1999. International Code of Zoological Nomenclature, Fourth Edition: adopted by the International Union of Biological Sciences. The International Trust for Zoological Nomenclature. Available from https://www.iczn.org/the-code/the-international-code-of-zoological-nomenclature/the-code-online/ [accessed 16 Dec. 2022].

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A. & Jermiin L.S. 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P. & Drummond A. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (12): 1647–1649. https://doi.org/10.1093/bioinformatics/bts199

Kilpatrick S.K., Gibbs J., Mikulas M.M., Spichiger S.-E., Ostiguy N., Biddinger D.J. & López-Uribe M.M. 2020. An updated checklist of the bees (Hymenoptera, Apoidea, Anthophila) of Pennsylvania, United States of America. Journal of Hymenoptera Research 77: 1–86. https://doi.org/10.3897/jhr.77.49622

Kohlschütter C. [Internet]. Fuzzy Gazetteer. Available from http://isodp.hof-university.de/fuzzyg/query/ [accessed 21 Oct. 2021].

Krombein K.V. 1967. Superfamily Apoidea. In: Krombein K.V. & Burks B.D. (eds) Hymenoptera of America North of Mexico–Synoptic Catalog, Second Supplement. United States Department of Agriculture, Washington, D.C. https://doi.org/10.5962/bhl.title.63670

Maddison W.P. & Maddison D.R. 2019. Mesquite: a modular system for evolutionary analysis ver. 3.61. Available from http://www.mesquiteproject.org [accessed 26 Dec. 2019].

Magnacca K.N., Gibbs J. & Droege S. 2013. Notes on alien and native bees (Hymenoptera: Apoidea) from the Hawaiian Islands. Bishop Museum Occasional Papers 114: 61–65.

Michener C.D. 1936. Some bees of the genus Halictus. Journal of Natural History 18 (104): 281–287. https://doi.org/10.1080/00222933608655192

Michener C.D. 1937. Records and descriptions of North American bees. Journal of Natural History 19 (111): 313–329. https://doi.org/10.1080/00222933708655269

Michener C.D. 1951. Superfamily Apoidea. In: Muesebeck C.F.W., Krombein K.V. & Townes H.K. (eds) Hymenoptera of America North of Mexico Synoptic Catalog: 1043–1255. United States Government Printing Office, Washington, D.C.

Michener C.D. 1954. Bees of Panamá. Bulletin of the American Museum of Natural History 104 (1): 1–176.

Michener C.D. 2007. The Bees of the World. The Johns Hopkins University Press, Baltimore, MD.

Minckley R.L. 2008. Faunal composition and species richness differences of bees (Hymenoptera: Apiformes) from two north American regions. Apidologie 39 (1): 176–188. https://doi.org/10.1051/apido:2007062

Mitchell T.B. 1960. Bees of the eastern United States, Volume I. North Carolina Agricultural Experiment Station Technical Bulletin 141: 1–538.

Moure J.S. & Hurd P.D. 1987. An Annotated Catalog of the Halictid Bees of the Western Hemisphere (Hymenoptera: Halictidae). Smithsonian Institution Press, Washington, D.C.

Patten M.M., Carioscia S.A. & Linnen C.R. 2015. Biased introgression of mitochondrial and nuclear genes: a comparison of diploid and haplodiploid systems. Molecular Ecology 24: 5200–5210. https://doi.org/10.1111/mec.13318

Pfau H.K. 2018. Functional morphology of the mesothoracic flight apparatus of Apis mellifera (Hymenoptera: Apidae). Entomologia Generalis 37 (3–4): 353–373. https://doi.org/10.1127/entomologia/2018/0652

Phillips S.J., Dudík M. & Schapire R.E. [Internet]. Maxent software for modeling species niches and distributions. ver. 3.4.1. Available from http://biodiversityinformatics.amnh.org/open_source/maxent/ [accessed 9 May 2020].

Phillips S.J., Anderson R.P. & Schapire R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

Phillips S.J., Anderson R.P., Dudík M., Schapire R.E. & Blair M.E. 2017. Opening the black box: an open-source release of Maxent. Ecography 40: 887–893. https://doi.org/10.1111/ecog.03049

QGIS.org. 2020. QGIS Geographic Information System. ver. 3.12. Available from http://qgis.org [accessed 8 May 2020].

R Core Team. 2020. R: A Language and Environment for Statistical Computing. ver. 4.0.0. Available from http://www.R-project.org [accessed 8 May 2020].

Ratnasingham S. & Hebert P.D.N. 2007. BOLD: the Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7 (3): 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x

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

Robertson C. 1890. New North American bees of the genera Halictus and Prosopis. Transactions of the American Entomological Society 17 (4): 315–318.

Robertson C. 1902. Synopsis of Halictinae. The Canadian Entomologist 34 (9): 243–250. https://doi.org/10.4039/Ent34243-9

Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., 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

Sandhouse G.A. 1923. The bee-genus Dialictus. The Canadian Entomologist 55 (8): 193–195. https://doi.org/10.4039/Ent55193-8

Sandhouse G.A. 1924. New North American species of bees belonging to the genus Halictus (Chloralictus). Proceedings of the United States National Museum 65 (19): 1–43. https://doi.org/10.5479/si.00963801.2532

Scott V.L., Ascher J.S., Griswold T.L. & Nufio C.R. 2011. The bees of Colorado. Natural History Inventory of Colorado 23: 1–100.

Snodgrass R.E. 1935. Principles of Insect Morphology. McGraw-Hill Book Company, New York.

Tabor J.A. & Koch J.B. 2021. Ensemble models predict invasive bee habitat suitability will expand under future climate scenarios in Hawai’i. Insects 12 (5): 443. https://doi.org/10.3390/insects12050443

Viereck H.L., MacGillivray A.D., Brues C.T., Wheeler W.M. & Rohwer S.A. 1916. The Hymenoptera, or wasp-like insects, of Connecticut. In: Britton W.E. (ed.) Guide to the Insects of Connecticut: 824. Connecticut Geological and Natural History Survey, Hartford, CT.

WFO. 2022. World Flora Online. Available from http://www.worldfloraonline.org [accessed 6 Jan. 2022].

Wiley E.O. & Mayden R.L. 2000. The evolutionary species concept. In: Wheeler Q.D. & Meier R. (eds) Species Concepts and Phylogenetic Theory: A Debate: 70–89. Columbia University Press, New York.

Wolf A.T. & Ascher J.S. 2009. Bees of Wisconsin (Hymenoptera: Apoidea: Anthophila). Great Lakes Entomologist 41: 129–168.

Published
2023-02-10
How to Cite
Gardner, J., & Gibbs, J. (2023). Revision of the Nearctic species of the Lasioglossum (Dialictus) gemmatum species complex (Hymenoptera: Halictidae). European Journal of Taxonomy, 858(1), 1-222. https://doi.org/10.5852/ejt.2023.858.2041
Section
Monograph