Bumblebees of the hypnorum-complex world-wide including two new near-cryptic species (Hymenoptera: Apidae)
Abstract
The hypnorum-complex of bumblebees (in the genus Bombus Latreille, 1802) has been interpreted as consisting of a single widespread Old-World species, Bombus hypnorum (Linnaeus, 1758) s. lat., and its closely similar sister species in the New World, B. perplexus Cresson, 1863. We examined barcodes for evidence of species’ gene coalescents within this species complex, using the closely related vagans-group to help calibrate Poisson-tree-process models to a level of branching appropriate for discovering species. The results support seven candidate species within the hypnorum-complex (Bombus taiwanensis Williams, Sung, Lin & Lu, 2022, B. wolongensis Williams, Ren & Xie sp. nov., B. bryorum Richards, 1930, B. hypnorum, B. koropokkrus Sakagami & Ishikawa, 1972, and B. hengduanensis Williams, Ren & Xie sp. nov., plus B. perplexus), which are comparable in status to the currently accepted species of the vagans-group. Morphological corroboration of the coalescent candidate species is subtle but supports the gene coalescents if these candidates are considered near-cryptic species.
References
An J.-D., Huang J.-X., Shao Y.-Q., Zhang S.-W., Wang B., Liu X.-Y., Wu J. & Williams P.H. 2014. The bumblebees of North China (Apidae, Bombus Latreille). Zootaxa 3830: 1–89. https://doi.org/10.11646/zootaxa.3830.1.1
Baker A.J., Tavares E.S. & Elbourne R.F. 2009. Countering criticisms of single mitochondrial DNA gene barcoding in birds. Molecular Ecology Resources: 9 (supplement 1): 257–268. https://doi.org/10.1111/j.1755-0998.2009.02650.x
Barrowclough G.F. 1982. Geographic variation, predictiveness, and subspecies. Auk 99: 601–603.
Baum D. & Smith S. 2012. Tree thinking: an introduction to phylogenetic biology. Roberts and Company, Greenwood Village, USA.
Biella P., Cetkovic A., Gogala A., Neumayer J., Sarospataki M., Sima P. & Smetana V. 2020. Northwestward range expansion of the bumblebee Bombus haematurus into Central Europe is associated with warmer winters and niche conservatism. Insect Science 28: 861–872.
Cameron S.A., Hines H.M. & Williams P.H. 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biological Journal of the Linnean Society 91: 161–188.
Chiu S.C. 1948. Revisional notes on the Formosan bombid-fauna (Hymenoptera). Notes d’entomologie chinoise 12: 57–81.
Cresson E.T. 1863. List of the North American species of Bombus and Apathus. Proceedings of the Entomological Society of Philadelphia 2: 83–116.
Cresson E.T. 1916 The Cresson types of Hymenoptera. Memoirs of the American Entomological Society 1: 1–141.
Crowther L.P., Hein P.-L. & Bourke A.F.G. 2014. Habitat and forage associations of a naturally colonising insect pollinator, the tree bumblebee Bombus hypnorum. PLoS ONE 9: e107568. https://doi.org/10.1371/journal.pone.0107568
de Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886.
Dellicour S. & Flot J.-F. 2015. Delimiting species-poor data sets using single molecular markers: a case study of barcode gaps, haplowebs and GMYC. Systematic Biology 64 (6): 900–908. https://doi.org/10.1093/sysbio/syu130
Dellicour S., Michez D. & Mardulyn P. 2015. Comparative phylogeography of five bumblebees: impact of range fragmentation, range size and diet specialization. Biological Journal of the Linnean Society 116: 926–939. https://doi.org/10.1111/bij.12636
Dellicour S., Kastally C., Varela, S., Michez D., Rasmont P., Mardulyn P. & Lecocq T. 2017. Ecological niche modelling and coalescent simulations to explore the recent geographical range history of five widespread bumblebee species in Europe. Journal of Biogeography 44: 39–50. https://doi.org/10.1111/jbi.12748
Drummond A.J. & Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BioMed Central Evolutionary Biology 7: 214. https://doi.org/10.1186/1471-2148-7-214
Erichson W.F. 1851. Hymenoptera. In: Middendorff A.T.v. (ed.) Reise in den Äussersten Norden und Osten Sibiriens, während der Jahre 1843 und 1844 mit allerhöchster Genehmigung auf Veranstaltung der kaiserlichen Akademie der Wissenschaften zu St. Petersburg ausgeführt und in Verbindung mit vielen Gelehrten herausgegeben. Band II. Zoologie. Theil 1: 60–65. Buchdruckerei der Kaiserlichen Akademie der Wissenschaften, St Petersburg. Available from https://www.biodiversitylibrary.org/page/37047877#page/74/mode/1up [accessed 8 Nov. 2022].
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
Goulson D. & Williams P. 2001. Bombus hypnorum (Hymenoptera: Apidae), a new British bumblebee? British Journal of Entomology and Natural History 14: 129–131.
Hebert P.D.N., Cywinska A., Ball S.L. & DeWaard J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, Biological Sciences 270: 313–321. https://doi.org/10.1098/rspb.2002.2218
Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H. & Hallwachs W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101: 14812–14817. https://doi.org/10.1073/pnas.0406166101
Hines H.M., Cameron S.A. & Williams P.H. 2006. Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera: Apidae: Bombus) with insights into gene utility for lower-level analysis. Invertebrate Systematics 20: 289–303. https://doi.org/10.1071/IS05028
Huml J.V., Ellis J.S., Lloyd K., Benefer C.M., Kiernan M., Brown M.J.F. & Knight M.E. 2021. Bucking the trend of pollinator decline: the population genetics of a range expanding bumblebee. Evolutionary Ecology 35: 413–442. https://doi.org/10.1007/s10682-021-10111-2
Hyde K.D. & Zhang Y. 2008. Epitypification: should we epitypify? Journal of Zhejiang University SCIENCE B 9: 842–846. https://doi.org/10.1631/jzus.b0860004
ICZN 1999. International Code of Zoological Nomenclature. 4th Edition. London, U.K. International Trust for Zoological Nomenclature. London, UK. Available from https://www.iczn.org/the-code/ [accessed 3 Nov. 2022].
Lecocq T., Dellicour S., Michez D., Lhomme P., Vanderplanck M., Valterova I., Rasplus J.-Y. & Rasmont P. 2013. Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BMC Evolutionary Biology 13: 263. https://doi.org/10.1186/1471-2148-13-263
Lecocq T., Gérard M., Michez D. & Dellicour S. 2016. Conservation genetics of European bees: new insights from the continental scale. Conservation Genetics 18: 585–596. https://doi.org/10.1007/s10592-016-0917-3
Lecocq T., Biella P., Martinet B. & Rasmont P. 2019. Too strict or too loose? Integrative taxonomic assessment of Bombus lapidarius complex (Hymenoptera: Apidae). Zoologica Scripta 49 (2): 187–196. https://doi.org/10.1111/zsc.12402
Leliaert F., Verbruggen H., Vanormelingen P., Steen F., Lopez-Bautista J.M., Zuccarello G.C. & de Clerck O. 2014. DNA-based species delimitation in algae. European Journal of Phycology 49: 179–196. https://doi.org/10.1080/09670262.2014.904524
Linnaeus C. 1758. Systema Naturae. Editio Decima, Reformata. Salvus, Holmiae [Stockholm]. Available from https://www.biodiversitylibrary.org/item/10277#page/3/mode/1up [accessed 1 Nov. 2022].
Løken A. 1973. Studies on Scandinavian bumble bees (Hymenoptera, Apidae). Norsk entomologisk Tidsskrift 20: 1–218.
Magnacca K.N. & Brown M.J.F. 2010. Mitochondrial heteroplasmy and DNA barcoding in Hawaiian Hylaeus (Nesoprosopis) bees (Hymenoptera: Colletidae). BMC Evolutionary Biology 10: 174. https://doi.org/10.1186/1471-2148-10-174
Martinet B., Ghisbain G., Przybyla K., Zambra E., Brasero N., Kondakov A.V., Tomilova A.A., Kolosova Y.S., Bolotov I.N., Rasmont P. & Potapov G. 2021. Distant but related: genetic structure in the circum boreal bumblebee Bombus jonellus (Kirby, 1802). Polar Biology 44 (10): 2039–2047. https://doi.org/10.1007/s00300-021-02937-x
Michener C.D. 2000. The Bees of the World. John Hopkins University Press, Baltimore.
O’Donnell M. 2018. Tree bumblebee (Bombus hypnorum) (Hymenoptera, Apidae): a bumblebee new to Ireland. The Irish Naturalists’ Journal: 36: 50–51. https://www.jstor.org/stable/45181554
Phillips J.D., Gillis D.J. & Hanner R.H. 2018. Incomplete estimates of genetic diversity within species: implications for DNA barcoding. Ecology and Evolution: Ecology and Evolution 9 (5): 2996–3010. https://doi.org/10.1002/ece3.4757
Prŷs-Jones O.E. 2014. The tree bumble bee (Bombus hypnorum) as a house sparrow equivalent? Comments on colonizing success in Britain in the context of declining native species. Bee World 91: 98–101. https://doi.org/10.1080/0005772X.2014.11417623
Prŷs-Jones O. 2019. Preadaptation to the vertical: an extra dimension to the natural history and nesting habits of the Tree Bumble Bee, Bombus (Pyrobombus) hypnorum. Journal of Apicultural Research 58: 643–659. https://doi.org/10.1080/00218839.2019.1634462
Prŷs-Jones O.E., Kristjansson K. & Olafsson E. 2016. Hitchhiking with the Vikings? The anthropogenic bumblebee fauna of Iceland – past and present. Journal of Natural History 50: 2895–2916. https://doi.org/10.1080/00222933.2016.1234655
Rasmont P. 1984. Les bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae). Spixiana 7: 135–160. Available from https://www.biodiversitylibrary.org/part/66953 [accessed 8 Nov. 2022].
Rasmont P. 1988. Monographie Écologique et Zoogéographique des Bourdons de France et de Belgique (Hymenoptera, Apidae, Bombinae). Faculté des Sciences agronomiques de l’Etat, Gembloux.
Rasmont P., Ghisbain G. & Terzo M. 2021. Bumblebees of Europe and Neighbouring Regions. NAP Editions, Verrières-le-Buisson, France.
Ratnasingham S. & Hebert P.D.N. 2007. BOLD: The Barcode Of Life Data system (http://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. PLoSONE 8 (8): e66213. https://doi.org/10.1371/journal.pone.0066213
Reid N.M. & Carstens B.C. 2012. Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology 12: 196. https://doi.org/10.1186/1471-2148-12-196
Reinig W.F. 1939. Die Evolutionsmechanismen, erläutert an den Hummeln. Verhandlungen der Deutschen zoologischen Gesellschaft (Supplement) 12: 170–206.
Richards O.W. 1930. The humble-bees captured on the expeditions to Mt. Everest (Hymenoptera, Bombidae). Annals and Magazine of Natural History (Series 10) 5: 633–658. https://doi.org/10.1080/00222933008673177
Richards O.W. 1934. Some new species and varieties of oriental humble-bees (Hym. Bombidae). Stylops 3: 87–90. https://doi.org/10.1111/j.1365-3113.1934.tb01552.x
Ronquist F. & Huelsenbeck J.P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Sakagami S.F. & Ishikawa R. 1969. Note préliminaire sur la répartition géographique des bourdons japonais, avec descriptions et remarques sur quelques formes nouvelles ou peu connues. Journal of the Faculty of Science, Hokkaido University (Zoology) 17: 152–196. Available from http://hdl.handle.net/2115/27480 [accessed 9 Nov. 2022].
Sakagami S.F. & Ishikawa R. 1972. Note supplémentaire sur la taxonomie et répartition géographique de quelques bourdons Japonais, avec la description d’une nouvelle sous-espèce. Bulletin of the National Science Museum, Tokyo: 15: 607–616.
Schlick-Steiner B.C., Steiner F.M., Seifert B., Stauffer C., Christian E. & Crozier R.H. 2010. Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55: 421–438. https://doi.org/10.1146/annurev-ento-112408-085432
Smith F. 1861. Descriptions of new genera and species of exotic Hymenoptera. Journal of Entomology 1: 146–155.
Starr C.K. 1992. The bumble bees (Hymenoptera: Apidae) of Taiwan. Bulletin of the National Museum of Natural Science 3: 139–157.
Stephen W.P. 1957. Bumble bees of western America (Hymenoptera: Apoidea). Technical Bulletin, Oregon State College, Agricultural Experiment Station 40: 163.
Talavera G., Dinca V. & Vila R. 2013. Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. Methods in Ecology and Evolution 4: 1101–1110. https://doi.org/10.1111/2041-210X.12107
Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
Thorp R.W., Horning D.S. & Dunning L.L. 1983. Bumble bees and cuckoo bumble bees of California (Hymenoptera: Apidae). Bulletin of the California Insect Survey 23: 79.
Tkalců B. 1974. Eine Hummel-Ausbeute aus dem Nepal-Himalaya (Insecta, Hymenoptera, Apoidea, Bombinae). Senckenbergiana biologica 55: 311–349.
Williams P.H. 1985. A preliminary cladistic investigation of relationships among the bumble bees (Hymenoptera, Apidae). Systematic Entomology 10: 239–255. https://doi.org/10.1111/j.1365-3113.1985.tb00529.x
Williams P.H. 1991. The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bulletin of the British Museum of the Natural History Museum Entomology 60: 1–204. Available from https://www.researchgate.net/publication/230668921 [accessed 1 Nov. 2022].
Williams P.H. 1994. Phylogenetic relationships among bumble bees (Bombus Latr.): a reappraisal of morphological evidence. Systematic Entomology 19: 327–344. https://doi.org/10.1111/j.1365-3113.1994.tb00594.x
Williams P.H. 1998. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of the British Museum of the Natural History Museum Entomology 67: 79–152 [update available from https://www.nhm.ac.uk/bombus/, accessed 3 Nov. 2022]. Available from https://www.researchgate.net/publication/230668913 [accessed 3 Nov. 2022].
Williams P.H. 2007. The distribution of bumblebee colour patterns world-wide: possible significance for thermoregulation, crypsis, and warning mimicry. Biological Journal of the Linnean Society 92: 97–118. https://doi.org/10.1111/j.1095-8312.2007.00878.x
Williams P.H. 2021. Not just cryptic, but a barcode bush: PTP re-analysis of global data for the bumblebee subgenus Bombus s. str. supports additional species (Apidae, genus Bombus). Journal of Natural History 55: 271–282. https://doi.org/10.1080/00222933.2021.1900444
Williams P.H. 2022a. The Bumblebees of the Himalaya. AbcTaxa, Belgium. Available from https://www.researchgate.net/publication/361184342 [accessed 11 Nov. 2022].
Williams P.H. 2022b. Novel splitting/lumping index reflects the history of species concepts applied to bumblebees (Insecta, Apidae). Zoological Journal of the Linnean Society: 196 (2): 704–719. https://doi.org/10.1093/zoolinnean/zlab123
Williams P.H., Cameron S.A., Hines H.M., Cederberg B. & Rasmont P. 2008. A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie 39: 46–74. https://doi.org/10.1051/apido:2007052
Williams P.H., Colla S. & Xie Z.-H. 2009a. Bumblebee vulnerability: common correlates of winners and losers across three continents. Conservation Biology 23: 931–940. https://doi.org/10.1111/j.1523-1739.2009.01176.x
Williams P.H., Tang Y., Yao J. & Cameron S. 2009b. The bumblebees of Sichuan (Hymenoptera: Apidae, Bombini). Systematics and Biodiversity 7: 101–189. https://doi.org/10.1017/S1477200008002843
Williams P.H., Ito M., Matsumura T. & Kudo I. 2010. The bumblebees of the Nepal Himalaya (Hymenoptera: Apidae). Insecta Matsumurana: 66: 115–151. Available from http://hdl.handle.net/2115/44628 [accessed 9 Nov. 2022].
Williams P.H., Brown M.J.F., Carolan J.C., An J.-D., Goulson D., Aytekin A.M., Best L.R., Byvaltsev A.M., Cederberg B., Dawson R., Huang J.-X., Ito M., Monfared, A., Raina R.H., Schmid-Hempel P., Sheffield C.S., Sima P. & Xie Z.-H. 2012. Unveiling cryptic species of the bumblebee subgenus Bombus s. str. world-wide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity 10: 21–56. https://doi.org/10.1080/14772000.2012.664574
Williams P.H., Thorp R.W., Richardson L.L. & Colla S.R. 2014. Bumble Bees of North America. An Identification Guide. Princeton University Press, Princeton, New Jersey.
Williams P.H., Byvaltsev A.M., Cederberg B., Berezin M.V., Ødegaard F., Rasmussen C., Richardson L.L., Huang J.-X., Sheffield C.S. & Williams S.T. 2015. Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE 10 (12): e0144544.. https://doi.org/10.1371/journal.pone.0144544
Williams P.H., Huang J.-X., Rasmont P. & An J.-D. 2016. Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species’ gene coalescents and morphology (Hymenoptera, Apidae). Zootaxa 4204: 1–72. https://doi.org/10.11646/zootaxa.4204.1.1
Williams P.H., Huang J.-X. & An J.-D. 2017. Bear wasps of the Middle Kingdom: a decade of discovering China’s bumblebees. Antenna 41: 21–24. Available from http://hdl.handle.net/10141/622626 [accessed 9 Nov. 2022].
Williams P.H., Altanchimeg D., Byvaltsev A., De Jonghe R., Jaffar S., Japoshvili G., Kahono S., Liang H., Mei M., Monfared A., Nidup T., Raina R., Ren Z., Thanoosing C., Zhao Y. & Orr M.C. 2020. Widespread polytypic species or complexes of local species? Revising bumblebees of the subgenus Melanobombus world-wide (Hymenoptera, Apidae, Bombus). European Journal of Taxonomy 719: 1–120. https://doi.org/10.5852/ejt.2020.719.1107
Williams P.H., Sung I.-H., Lin Y.-J. & Lu S.-S. 2022. Discovering endemic species among the bumblebees of Taiwan (Apidae, genus Bombus). Journal of Natural History 56: 435–447. https://doi.org/10.1080/00222933.2022.2052991
Wilson E.O. & Brown W.L. 1953. The subspecies concept and its taxonomic application. Systematic Zoology 2: 97–111. https://doi.org/10.2307/2411818
Zhang J.-J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876. https://doi.org/10.1093/bioinformatics/btt499
Zink R.M. 2004. The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society of London (B): 271: 561–564. https://doi.org/10.1098/rspb.2003.2617
Copyright (c) 2022 Paul H. Williams, Phurpa Dorji, Zongxin Ren, Zhenghua Xie, Michael Orr
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:
- 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.
- 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.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.
