Widespread polytypic species or complexes of local species? Revising bumblebees of the subgenus Melanobombus world-wide (Hymenoptera, Apidae, Bombus)

  • Paul H. Williams Natural History Museum, Cromwell Road, London SW7 5BD https://orcid.org/0000-0002-6996-5682
  • Dorjsuren Altanchimeg Institute of General and Experimental Biology, Peace Avenue 54b, Ulaanbaatar 13330
  • Alexandr Byvaltsev Novosibirsk State University, ul. Pirogova 2, Novosibirsk 630090 https://orcid.org/0000-0001-6555-5646
  • Roland De Jonghe Langstraat 105, B-2260 Westerlo
  • Saleem Jaffar https://orcid.org/0000-0002-7664-7869
  • George Japoshvili Agricultural University of Georgia, 240 Agmashenebli Alley, Tbilisi https://orcid.org/0000-0002-9901-4554
  • Sih Kahono Indonesian Institute of Sciences (LIPI), Jakarta
  • Huan Liang Kunming Institute of Botany (Chinese Academy of Sciences), 132 Lanhei Road, Kunming, Yunnan 650201
  • Maurizio Mei Università di Roma ‘Sapienza’, Piazzale Valerio Massimo 6, Roma 00162
  • Alireza Monfared Yasouj University, Zirtol, Yasouj https://orcid.org/0000-0002-4465-3228
  • Tshering Nidup Sherubtse College, Royal University of Bhutan, Trashigang https://orcid.org/0000-0001-8802-0345
  • Rifat Raina Zoological Survey of India, Pali Road, Jodhpur 342005, Rajasthan
  • Zongxin Ren Kunming Institute of Botany (Chinese Academy of Sciences), 132 Lanhei Road, Kunming, Yunnan 650201
  • Chawatat Thanoosing Natural History Museum, Cromwell Road, London SW7 5BD https://orcid.org/0000-0002-4228-748X
  • Yanhui Zhao Kunming Institute of Botany (Chinese Academy of Sciences), 132 Lanhei Road, Kunming, Yunnan 650201
  • Michael C. Orr Institute of Zoology (Chinese Academy of Sciences), 1 Beichen West Road, Chaoyang, Beijing 100101
Keywords: barcode, bumblebee, coalescent, distribution, species


Species are often presumed to be apparent in nature, but in practice they may be difficult to recognise, especially when viewed across continents rather than within a single site. Coalescent-based Poisson-tree-process (PTP) models applied to fast-evolving genes promise one quantitative criterion for recognising species, complete with the estimates of uncertainty that are required of a scientific method. Such methods face challenges especially in discerning between widespread polytypic species and complexes of closely related, restricted-range species. In particular, ‘over-sampling’ of many closely related individuals within one species could risk causing groups of less closely-related individuals within other species appearing relatively more distinct and consequently could risk them being interpreted falsely as separate species. Some of the most persistent taxonomic problems among bumblebees (genus Bombus Latreille, 1802) are within the subgenus Melanobombus von Dalla Torre, 1880. For a global revision of Melanobombus species, we use COI barcodes and seek to reduce the risk from localised over-sampling by filtering the data to include only unique haplotypes. Unique haplotypes give more conservative results than unfiltered data, but still increase the number of species in comparison with recent morphological treatments. After integrative assessment of COI coalescents in comparison with morphological groups, the number of accepted species shows a non-linear increase with sample size that plateaus to an increase of 47% (to 25 species) compared with a previous estimate (of 17) based on morphology alone. For the most widespread and variable species-complexes, our revised species improve the match to the patterns expected of species, both for genetic divergence-with-distance and for sympatry, leading to three main inferences. (1) The particularly widespread polytypic Bombus sichelii Radoszkowski, 1859, is a single species. (2) We detect two candidates for species within previous broad concepts of each of the former B. lapidarius (Linnaeus, 1758), B. miniatus Bingham, 1897, and B. rufofasciatus Smith, 1852. Within B. lapidarius s. lat. we find insufficient evidence to corroborate the candidate species, with no coalescent or morphological support for a recent claim for a separate species, B. bisiculus Lecocq, Biella, Martinet & Rasmont, 2019 described from southern Italy, but rather we find a weak and uncorroborated coalescent for a different and much broader group of samples from across southeastern Europe but excluding Turkey. Within the former broad concepts of B. miniatus s. lat. and B. rufofasciatus s. lat. the coalescent evidence is stronger and subtle evidence from morphology corroborates recognising B. miniatus s. str. and B. eurythorax Wang, 1892 stat. rev. as separate species as well as B. rufofasciatus s. str. and B. prshewalskyi Morawitz, 1880 stat. rev. as separate species. (3) Our coalescent and morphological results ‘split’ more clearly what has long been interpreted as a single polytypic B. keriensis Morawitz, 1887, s. lat., by supporting novel concepts of the restricted-range species: B. alagesianus Reinig, 1930 stat. rev., B. incertoides Vogt, 1911 stat. rev., B. keriensis s. str., B. qilianensis sp. nov., B. separandus Vogt, 1909 stat. rev., and B. tibeticus sp. nov. A lectotype is designated for the name B. keriensis and a neotype is designated for the name B. alagesianus. We estimate the phylogeny of Melanobombus species by including three slower-evolving genes to provide more evidence for deeper relationships, to estimate the time calibration of this phylogeny, and to estimate ancestral distributions, all within a Bayesian framework. We provide the first keys for identifying all of the species of Melanobombus.


Alford D.V. 1975. Bumblebees. Davis-Poynter, London.

Almeida E.A.B., Packer L., Melo G.A.R., Danforth B.N., Cardinal S.C., Quinteiro F.B. & Pie M.R. 2018. The diversification of neopasiphaeine bees during the Cenozoic (Hymenoptera: Colletidae). Zoologica Scripta 48 (2): 226–242. https://doi.org/10.1111/zsc.12333

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

Ball F.J. 1920. Notes supplementaires sur les bourdons de la Belgique. Annales de la Société entomologique de Belgique 60: 31–43.

Barraclough T.G. & Vogler A.P. 2000. Detecting the geographical pattern of speciation from species-level phylogenies. American Naturalist 155: 419–434. https://doi.org/10.1086/303332

Barrowclough G.F. 1982. Geographic variation, predictiveness, and subspecies. The Auk 99: 601–603.

Baum D. & Smith S. 2012. Tree Thinking: an Introduction to Phylogenetic Biology. Roberts and Company, Greenwood Village, CO, USA.

Benoist R. 1928. Bombus lapidarius L. st. atlanticus R. Ben. Bulletin de la Société des sciences naturelles du Maroc 1927: 212.

Benton T. 2006. Bumblebees, the Natural History & Identification of the Species Found in Britain. Collins, London.

Berezin M.V., Beiko V.B. & Berezina N.V. 1996. Analysis of structural changes in the bumblebee (Bombus, Apidae) population of Moscow Oblast over the last forty years. Entomological Review 76: 115–123

Bertsch A. 2010. A phylogenetic framework for the bumblebee species of the subgenus Bombus sensu stricto based on mitochondrial DNA markers, with a short description of the neglected taxon B. minshanicola Bischoff, 1936 n. status. Beiträge zur Entomologie 60: 471–487. https://doi.org/10.21248/contrib.entomol.60.2.471-487

Bertsch A., Schweer H. & Titze A. 2004. Discrimination of the bumblebee species Bombus lucorum, B. cryptarum and B. magnus by morphological characters and male labial gland secretions. Beiträge zur Entomologie 54: 365–386. https://doi.org/10.21248/contrib.entomol.54.2.365-386

Bertsch A., Schweer H., Titze A. & Tanaka H. 2005. Male labial gland secretions and mitochondrial DNA markers support species status of Bombus cryptarum and B. magnus (Hymenoptera, Apidae). Insectes sociaux 52: 45–54. https://doi.org/10.1007/s00040-004-0761-1

Bertsch A., Habré de Angelis M. & Przemeck G.K.H. 2010. Phylogenetic relationships of the bumblebees Bombus moderatus, B. albocinctus, B. burjaeticus, B. florilegus and B. cryptarum based on mitochondrial DNA markers: a complex of closely related taxa with circumpolar distribution. Beiträge zur Entomologie 60: 13–32. https://doi.org/10.21248/contrib.entomol.60.1.13-32

Bingham C.T. 1897. The Fauna of British India, including Ceylon and Burma. Hymenoptera. Vol. I. Wasps and Bees. Taylor & Francis, London.

Bird M.I., Taylor D. & Hunt C. 2005. Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews 24: 2228–2242. https://doi.org/10.1016/j.quascirev.2005.04.004

Bischoff H. 1935. Genus BOMBUS (Apidae, Hymen.). In: Wissenschaftliche Ergebnisse der niederländischen Expedition in den Karakorum und die angrenzenden Gebiete in den Jahren 1922, 1925 und 1929/30: 255–256. C. Visser & J. Visser-Hooft, Leipzig.

Bischoff H. 1936. Schwedisch-chinesische wissenschaftliche Expedition nach den nordwestlichen Provinzen Chinas, unter Leitung von Dr. Sven Hedin und Prof. Sü Ping-chang. Insekten gesammelt vom schwedischen Arzt der Expedition Dr. David Hummel 1927-1930. 56. Hymenoptera. 10. Bombinae. Arkiv för zoologi 27A: 1–27.

Bolton B. 2007. How to conduct large-scale taxonomic revisions in Formicidae. In: Snelling R.R., Fisher B.L. & Ward P.S. (eds) Advances in Ant Systematics (Hymenoptera: Formicidae): Homage to E.O. Wilson - 50 Years of Contributions. Memoirs of the American Entomological Institute 80: 52–71.

Brasero N., Lecocq T., Martinet B., Valterova I., Urbanova K., De Jonghe R. & Rasmont P. 2017. Variability in sexual pheromones questions their role in bumblebee pre-mating recognition system. Journal of Chemical Ecology 44: 9–17. https://doi.org/10.1007/s10886-017-0910-4

Cameron S.A., Derr J.N., Austin A.D., Wooley J.B. & Wharton R.A. 1992. The application of nucleotide sequence data to phylogeny of the Hymenoptera: a review. Journal of Hymenoptera Research 1: 63–79.

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. https://doi.org/10.1111/j.1095-8312.2007.00784.x

Campillo L.C., Barley A.J. & Thomson R.C. 2020. Model-based species delimitation: are coalescent species reproductively isolated? Systematic Biology 69: 708–721. https://doi.org/10.1093/sysbio/syz072

Cardoso A., Serrano A. & Vogler A.P. 2009. Morphological and molecular variation in tiger beetles of the Cicindela hybrida complex: is an ‘integrative taxonomy’ possible? Molecular Ecology 18: 648–664. https://doi.org/10.1111/j.1365-294X.2008.04048.x

Carstens B.C., Pelletier T.A., Reid N.M. & Satler J.D. 2013. How to fail at species delimitation. Molecular Ecology 22: 4369–4383. https://doi.org/10.1111/mec.12413

Chesser R.T. & Zink R.M. 1994. Modes of speciation in birds: a test of Lynch’s method. Evolution 48: 490–497. https://doi.org/10.1111/j.1558-5646.1994.tb01326.x

Chiu S.C. 1948. Revisional notes on the Formosan bombid-fauna (Hymenoptera). Notes d’entomologie chinoise 12: 57–81.

Cockerell T.D.A. 1906. Descriptions and records of bees. – XII. Annals and Magazine of Natural History Series 7 18: 69–75. https://doi.org/10.1080/00222930608562581

Cockerell T.D.A. 1931. Bees obtained by Professor Claude R. Kellog in the Foochow district, China, with new records of Philippine Bombidae. American Museum Novitates 480: 1–7. Available from http://hdl.handle.net/2246/3030 [accessed 14 Aug. 2020].

Cracraft J. 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D. & Endler J.A. (eds) Speciation and its Consequences: 28–59. Sinauer Associates, Sunderland.

Cresson E.T. 1863. List of the North American species of Bombus and Apathus. Proceedings of the Entomological Society of Philadelphia 2: 83–116.

Darwin C. 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London. https://doi.org/10.5962/bhl.title.68064

Day M.C. 1979. The species of Hymenoptera described by Linnaeus in the genera Sphex, Chrysis, Vespa, Apis and Mutilla. Biological Journal of the Linnean Society 12: 45–84. https://doi.org/10.1111/j.1095-8312.1979.tb00049.x

De Meulemeester T. 2012. Approche intégrative dans la systématique de taxons complexes: bourdons et abeilles fossiles. PhD thesis, Université de Mons, France.

de Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886. https://doi.org/10.1080/10635150701701083

Dehon M., Engel M.S., Gerard M., Atytekin A.M., Ghisbain G., Williams P.H., Rasmont P. & Michez D. 2019. Morphometric analysis of fossil bumble bees (Hymenoptera, Apidae, Bombini) reveals their taxonomic affinities. Zookeys 891: 71–118. https://doi.org/10.3897/zookeys.891.36027

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

Dias B.S.F., Raw A. & Imperatri-Fonseca V.L. 1999. International Pollinators Initiative: the São Paulo Declaration on Pollinators. Report on the Recommendations of the Workshop on the Conservation and Sustainable Use of Pollinators in Agriculture with Emphasis on Bees. Brazilian Ministry of the Environment, Brasília. Available from https://www.pollinator.org/international [accessed 3 Sep. 2020].

Dillon R.T. 1984. Geographic distance, environmental difference, and divergence between isolated populations. Systematic Zoology 33: 69–82. https://doi.org/10.1093/sysbio/33.1.69

Dowton M. & Austin A.D. 1994. Molecular phylogeny of the insect order Hymenoptera: apocritan relationships. Proceedings of the National Academy of Sciences of the United States of America 91: 9911–9915. https://doi.org/10.1073/pnas.91.21.9911

Dray S. & Dufour A.-B. 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22: 1–20. https://doi.org/10.18637/jss.v022.i04

Drummond A.J. & Bouckaert R.R. 2015. Bayesian Evolutionary Analysis with BEAST. Cambridge University Press, Cambridge, UK. https://doi.org/10.1017/CBO9781139095112

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

Drummond A.J., Rambaut A. & Bouckaert R.R. 2013. Divergence dating tutorial with BEAST 2.0. https://doi.org/10.1371/journal.pcbi.1003537.s004

Duennes M.A., Petranek C., Díez de Bonilla E.P., Mérida-Rivas J., Martinez-López O., Sagot P., Vandame R. & Cameron S.A. 2017. Population genetics and geometric morphometrics of the Bombus ephippiatus species complex with implications for its use as a commercial pollinator. Conservation Genetics 18: 553–572. https://doi.org/10.1007/s10592-016-0903-9

Esmaili M. & Rastegar R. 1974. Identified species of aculeate Hymenoptera of Iran. Journal of the Entomological Society of Iran 2: 43–44 + [41–52].

Fabricius J.C. 1776. Genera Insectorum eorumque characteres naturales secundum numerum, figuram, situm et proportionem omnium partium oris adiecta mantissa specierum nuper detectarum. Bartsch, Kiel [Chilonii]. https://doi.org/10.5962/bhl.title.119827

Fourcroy A.F.d. 1785. Entomologia Parisiensis; sive Catalogus Insectorum quæ in agro Parisiensi reperiuntur; secundum methodum Geoffræanam in sectiones, genera & species distributus: cui addita sunt nomina trivialia & fere trecentæ novæ species. Paris. https://doi.org/10.5962/bhl.title.36528

Friese H. 1905. Neue oder wenig bekannte Hummeln des russischen Reiches (Hymenoptera). Ezhegodnik Zoologicheskago muzeya 9: 507–523.

Friese H. 1910. Neue Bienenarten aus Japan. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 60: 404–410.

Friese H. 1913. Über einige neue Apiden (Hym.). Archiv für Naturgeschichte 78: 85–89.

Friese H. 1914. Die Bienenfauna von Java. Tijdschrift voor Entomologie 57: 1–13.

Friese H. 1916. Über einige neue Hummelformen. Bombus 1916: 107–110.

Friese H. 1918. Wissenschaftlishe Ergebnisse einer Forschungsreise nach Ostindien, ausgeführt im Auftrage der Kgl. Preuss. Akademie der Wissenschaften zu Berlin von Herrn Prof. Dr. v. Buttel-Reepen. VII. Bienen aus Sumatra, Java, Malakka und Ceylon. Gesammelt von Herrn Prof. Dr. Buttel-Reepen in den Jahren 1911–1912. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Tiere 41: 489–520.

Frison T.H. 1923. Systematic and biological notes on bumblebees (Bremidae; Hymenoptera). Transactions of the American Entomological Society 48: 307–326. Available from https://www.jstor.org/stable/25077076 [accessed 14 Aug. 2020].

Frison T.H. 1930. The bumblebees of Java, Sumatra and Borneo (Bremidae: Hymenoptera). Treubia 12: 1–22.

Frison T.H. 1933. Records and descriptions of Bremus and Psithyrus from India (Bremidae: Hymenoptera). Record of the Indian Museum 35: 331–342.

Frison T.H. 1934. Records and descriptions of Bremus and Psithyrus from Formosa and the asiatic mainland. Transactions of the Natural History Society of Formosa 24: 150–185.

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

Ghiselin M. 1974. A radical solution to the species problem. Systematic Zoology 23: 536–544. https://doi.org/10.1093/sysbio/23.4.536

Goulson D. 2010. Bumblebees, Behaviour, Ecology, and Conservation, 2nd Ed. Oxford University Press, Oxford.

Gribodo G. 1892. Contribuzioni imenotterologiche. Sopra alcune specie nuove o poco conosciute di imenotteri antofili (generi Ctenoplectra, Xylocopa, Centris, Psithyrus, Trigona, e Bombus). Bolletino della Società Entomologica Italiana 23: 102–119.

Handlirsch A. 1888. Die Hummelsammlung des k. k. naturhistorischen Hofmuseums. Annalen des Naturhistorischen Museums in Wien 3: 209–250. Available from https://www.jstor.org/stable/41767613 [accessed 14 Aug. 2020].

Handlirsch A. 1891. Hummelstudien. Annalen des Naturhistorischen Museums in Wien 6: 446–454. Available from https://www.jstor.org/stable/41767691 [accessed 14 Aug. 2020].

Harris M. 1776. An Exposition of English Insects, with Curious Observations and Remarks, wherein each Insect is particularly described; its Parts and Properties considered; the different Sexes distinguished, and the natural History faithfully related. London. https://doi.org/10.5962/bhl.title.122956

Hasegawa M., Kishino H. & Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174. https://doi.org/10.1007/BF02101694

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. 2008. Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology 57: 58–75. https://doi.org/10.1080/10635150801898912

Hines H.M. & Williams P.H. 2012. Mimetic colour pattern evolution in the highly polymorphic Bombus trifasciatus (Hymenoptera: Apidae) species complex and its comimics. Zoological Journal of the Linnean Society 166: 805–826. https://doi.org/10.1111/j.1096-3642.2012.00861.x

Hoffer E. 1889. Die Schmarotzerhummeln Steiermarks. Lebensgeschichte und Beschreibung derselben. Mitteilungen des Naturwissenschaftlichen Vereins für Steiermark 25: 82–158.

Hull D.L. 1980. Individuality and selection. Annual Review of Ecology and Systematics 11: 311–332. https://doi.org/10.1146/annurev.es.11.110180.001523

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 Ed.. International Commission on Zoological Nomenclature, London. Available from https://www.iczn.org/the-code/the-international-code-of-zoological-nomenclature/the-code-online/ [accessed 14 Aug. 2020].

Ito M., Matsumura T. & Sakagami S.F. 1984. A nest of the Himalayan bumblebee Bombus (Festivobombus) festivus. Kontyu 52: 537–539.

Jackson J.M., Pimsler M.L., Oyen K.J., Koch-Uhuad J.B., Herndon J.D., Strange J.P., Dillon M.E. & Lozier J.D. 2018. Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude. Molecular Ecology 27: 2926–2942. https://doi.org/10.1111/mec.14735

Kapli P., Lutteropp S., Zhang J., Kobert K., Pavlidis P., Stamatakis A. & Flouri T. 2017. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33: 1630–1638. https://doi.org/10.1093/bioinformatics/btx025

Kato M., Salmah S. & Nagamitsu T. 1992. Colony cycle and foraging activity of a tropical-montane bumblebee, Bombus rufipes (Hymenoptera, Apidae) in Southeast Asia. Japanese Journal of Entomology 60: 765–776.

Kjellsson G., Rasmussen F.N. & Dupuy D. 1985. Pollination of Dendrobium infundibulum, Cymbidium insigne (Orchidaceae) and Rhododendron lyi (Ericaceae) by Bombus eximius (Apidae) in Thailand: a possible case of floral mimicry. Journal of Tropical Ecology 1: 289–302. https://doi.org/10.1017/S0266467400000389

Klug F. 1807. Species apiariarum familiae novas, descripsit, generumque characteres adjecit. Magazin der Gesellschaft Naturforschender Freunde zu Berlin 1: 263–265.

Knechtel W.K. 1963. Bombine din imprejurimile Lacului Petea (reg. Crisana). Communicarile Academiei Republicii Populare Romine 13: 711–715.

Knowles L.L. & Carstens B.C. 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56: 887–895. https://doi.org/10.1080/10635150701701091

Kriechbaumer J. 1873. Bemerkungen über einige Hummelarten. Stettiner entomologische Zeitung 34: 335–339.

Kuhlmann M. 2002. Neue Arten der Bienengattung Colletes Latr. aus Südtibet mit Beschreibung der Route der “Deutschen Tibet Expedition Ernst Schäfer 1938/9” (Hymenoptera: Apidae: Colletinae). Linzer biologische Beiträge 34: 1155–1178.

Lamm K.S. & Redelings B.D. 2009. Reconstructing ancestral ranges in historical biogeography: properties and prospects. Journal of Systematics and Evolution 47: 369–382. https://doi.org/10.1111/j.1759-6831.2009.00042.x

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., Brasero N., DeMeulemeester T., Michez D., Dellicour S., Lhomme P., de Jonghe R., Valterova I., Urbanova K. & Rasmont P. 2014. An integrative taxonomic approach to assess the status of Corsican bumblebees: implications for conservation. Animal Conservation 18: 236–248. https://doi.org/10.1111/acv.12164

Lecocq T., Dellicour S., Michez D., Dehon M., Dewulf A., De Meulemeester T., Brasero N., Valterova I., Rasplus J.-Y. & Rasmont P. 2015. Methods for species delimitation in bumblebees (Hymenoptera, Apidae, Bombus): towards an integrative approach. Zoologica Scripta 44: 281–297. https://doi.org/10.1111/zsc.12107

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: 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

Lepeletier de Saint-Fargeau A.L.M. [1835] 1836. Histoire naturelle des Insectes. Hyménoptères. Vol. 1. Librairie Enciclopédique de Roret, Paris. https://doi.org/10.5962/bhl.title.9005

Linnaeus C. 1758. Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis, Editio Decima, Reformata. Laurentii Salvii, Stockholm [Holmiae]. https://doi.org/10.5962/bhl.title.542

Lohse K. 2009. Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58: 439–442. https://doi.org/10.1093/sysbio/syp039

Maddison W.P. & Knowles L.L. 2006. Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55: 21–30. https://doi.org/10.1080/10635150500354928

Mallet J. 2013. Species, concepts of. In: Encyclopedia of Biodiversity, 2nd Ed: 679–691. Elsevier. https://doi.org/10.1016/B978-0-12-384719-5.00131-3

Mantel N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.

Mardulyn P. & Cameron S.A. 1999. The major opsin in bees (Insecta: Hymenoptera): a promising nuclear gene for higher level phylogenetics. Molecular Phylogenetics and Evolution 12: 168–176. https://doi.org/10.1006/mpev.1998.0606

Martinet B., Brasero N., Lecocq T., Biella P., Valterova I., Michez D. & Rasmont P. 2018a. Adding attractive semio-chemical trait refines the taxonomy of Alpinobombus (Hymenoptera: Apidae). Apidologie 49: 838–851. https://doi.org/10.1007/s13592-018-0611-1

Martinet B., Lecocq T., Brasero N., Biella P., Urbanova K., Valterova I., Cornalba M., Gjershaug J.O., Michez D. & Rasmont P. 2018b. Following the cold: geographical differentiation between interglacial refugia and speciation in the arcto-alpine species complex Bombus monticola (Hymenoptera: Apidae). Systematic Entomology 43: 200–217. https://doi.org/10.1111/syen.12268

Mason N.A., Fletcher N.K., Gill B.A., Funk W.C. & Zamudio K.R. 2020. Coalescent-based species delimitation is sensitive to geographic sampling and isolation by distance. Systematics and Biodiversity 18: 269–280. https://doi.org/10.1080/14772000.2020.1730475

Matzke N.J. 2013. Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers of Biogeography 5: 242–248. https://doi.org/10.21425/F55419694

Mayr E. 1963. Animal Speciation and Evolution. Harvard University Press, Cambridge, MA.

Meier R., Shiyang K., Vaidya G. & Ng P.K.L. 2006. DNA barcoding and taxonomy in Diptera: a tale of of high intraspecific variability and low identification success. Systematic Biology 55: 715–728. https://doi.org/10.1080/10635150600969864

Meyer C.P. & Paulay G. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3: e422. https://doi.org/10.1371/journal.pbio.0030422

Michener C.D. 2000. The Bees of the World. 1st Ed. John Hopkins University Press, Baltimore.

Michener C.D. & Amir M. 1977. The seasonal cycle and habitat of a tropical bumble bee. Pacific Insects 17: 237–240.

Monaghan M.T., Balke M., Gregory T.R. & Vogler A.P. 2005. DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society B 360: 1925–1933. https://doi.org/10.1098/rstb.2005.1724

Monaghan M.T., Wild R., Elliot M., Fujisawa T., Balke M., Inward D.J.G., Lees D.C., Ranaivosolo R., Eggleton P., Barraclough T.G. & Vogler A.P. 2009. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58: 298–311. https://doi.org/10.1093/sysbio/syp027

Morawitz F.F. 1880. Ein Beitrag zur Bienen-Fauna mittel-Asiens. Izvêstiya Imperatorskoi akademii nauk 26: 337–379.

Morawitz F.F. 1881. Die russischen Bombus-Arten in der Sammlung der Kaiserlichen Akademie der Wissenschaften. Izvêstiya Imperatorskoi akademii nauk 27: 213–265.

Morawitz F.F. 1887. Insecta in itinere cl. N. Przewalskii in Asia centrali novissime lecta. I. Apidae. Trudy Russkago éntomologicheskago obshchestva 20 (1886): 195–229.

Morawitz F.F. 1890. Insecta a cl. G. N. Potanin in China et in Mongolia novissime lecta. XIV. Hymenoptera Aculeata. II). III. Apidae. Trudy Russkago éntomologicheskago obshchestva 24: 349–385.

Neumayer J. & Paulus H.F. 1999. Ökologie alpiner Hummelgemeinscahften: Blütenbesuch, Ressourcenaufteilung und Energiehaushalt. Untersuchungen in den Ostalpen Österreichs. Stapfia 67: 5–246.

Niu Z.-Q., Yuan F. & Zhu C.-D. 2018. Species Catalogue of China. Volume 2 Animals. Insecta (IV). Apoidea (Apidae, Melittidae, Halictidae). Science Press, Beijing.

Özbek H. 1990. A new bumblebee species of Pyrobombus Dalla Torre (Hymenoptera, Apidae, Bombinae) in eastern Anatolia, Turkey. Türkiye entomoloji dergisi 14: 207–214.

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

Panzer G.W.F. 1805. Faunae Insectorum Germanicae initia oder Deutschlands Insecten gesammelt und herausgegeben. Nürnberg. https://doi.org/10.5962/bhl.title.15007

Papadopoulou A., Bergsten J., Fujisawa T., Monaghan M.T., Barraclough T.G. & Vogler A.P. 2008. Speciation and DNA barcodes: testing the effects of dispersal on the formation of discrete sequence clusters. Philosophical Transactions of the Royal Society B 363: 2987–2996. https://doi.org/10.1098/rstb.2008.0066

Papadopoulou A., Monaghan M.T., Barraclough T.G. & Vogler A.P. 2009. Sampling error does not invalidate the Yule-coalescent model for species delimitation. A response to Lohse (2009). Systematic Biology 58: 442–444. https://doi.org/10.1093/sysbio/syp038

Paterson H.E.H. 1985. The recognition concept of species. In: Vrba E.S. (ed.) Species and Speciation: 21–29. Pretoria.

Pendlebury H.M. 1923. Four new species of Bombus from the Malay Peninsula. Journal of the Federated Malay States Museums 11: 64–67.

Pérez J. 1890. Catalogue des mellifères du sud-ouest. Actes de la Société linnéenne de Bordeaux 44: 133–200.

Phillips J.D., Gillis D.J. & Hanner R.H. 2018. Incomplete estimates of genetic diversity within species: implications for DNA barcoding. Ecology and Evolution 9: 2996–3010. https://doi.org/10.1002/ece3.4757

Pittioni B. 1939a. Neue und wenig bekannte Hummeln der Paläarktis (Hymenopt., Apidae). Konowia 17: 244–263.

Pittioni B. 1939b. Tanguticobombus subg. nov. (Hymenopt., Apidae). Zoologischer Anzeiger 126: 201–205.

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: 595–609. https://doi.org/10.1080/10635150600852011

Potapov G.S., Kondakov A.V., Spitsyn V.M., Filippov B.Y., Kolosova Y.S., Zubril N.A. & Bolotov I.N. 2017. An integrative taxonomic approach confirms the valid status of Bombus glacialis, an endemic bumblebee species of the High Arctic. Polar Biology 41: 629–642. https://doi.org/10.1007/s00300-017-2224-y

Potapov G.S., Kondakov A.V., Filippov B.Y., Gofarov M.Y., Kolosova Y.S., Spitsyn V.M., Tomilova A.A., Zubril N.A. & Bolotov I.N. 2019. Pollinators on the polar edge of the Ecumene: taxonomy, phylogeography, and ecology of bumble bees from Novaya Zemlya. Zookeys 866: 85–115. https://doi.org/10.3897/zookeys.866.35084

Radoszkowski O. 1860. Sur quelques hyménoptères nouveaux ou peu connus de la collection du Musée de l’Académie des sciences de St. Pétersbourg. Byulleten’ Moskovskogo obshchestva ispytatelei prirody 32 (1859): 479–486.

Radoszkowski O. 1877. Séance du 3 (15) Mai 1876 [Preliminary diagnoses of two new species of Bombus]. Trudy Russkago éntomologicheskago obshchestva 13: vii–viii.

Radoszkowski O. 1883. Sur quelques espèces Russes appartenant au genre Bombus. Byulleten’ Moskovskogo obshchestva ispytatelei prirody 58: 168–226.

Radoszkowski O. 1884. Révision des armures copulatrices des mâles du genre Bombus. Byulletin’ Moskovskogo obshchestva ispytatelei prirody 59: 51–92.

Rasmont P. 1983. Catalogue commenté des bourdons de la région ouest-paléarctique (Hymenoptera, Apoidea, Apidae). Notes fauniques de Gembloux 7: 1–71.

Rasmont P. 1984. Les bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae). Spixiana 7: 135–160.

Rasmont P. 1988. Monographie écologique et zoogéographique des bourdons de France et de Belgique (Hymenoptera, Apidae, Bombinae). PhD Thesis, Faculté des Sciences agronomiques de l’Etat, Gembloux.

Rasmont P. & Flagothier D. 1996. Biogéographie et choix floraux des bourdons (Hymenoptera, Apidae) de la Turquie. Rapport preliminaire 1995–1996. In: NATO-OTAN TU-Pollination Project. Université de Mons-Hainaut, Mons, Belgium.

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

Rayfield D. 1976. The Dream of Lhasa. The Life of Nikolay Przhevalsky (1839-88), Explorer of Central Asia. Elek Books, London.

Ree R.H. & Sanmartín I. 2009. Prospects and challenges for parametric models in historical biogeographical inference. Journal of Biogeography 36: 1211–1220. https://doi.org/10.1111/j.1365-2699.2008.02068.x

Ree R.H. & Smith S.A. 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57: 4–14. https://doi.org/10.1080/10635150701883881

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. 1930. Untersuchungen zur Kenntnis der Hummelfauna des Pamir-Hochlandes. Zoologische Ergebnisse der deutsch-russischen Alai-Pamir-Expedition der Notgemeinschaft der Deutschen Wissenschaft und der Akademie der Wissenschaften der U.d.S.S.R. Zeitschrift für Morphologie und Ökologie der Tiere 17: 68–123.

Reinig W.F. 1935. On the variation of Bombus lapidarius L. and its cuckoo, Psithyrus rupestris Fabr., with notes on mimetic similarity. Journal of Genetics 30: 321–356. https://doi.org/10.1007/BF02982243

Reinig W.F. 1936. Beiträge zur Kenntnis der Hummelfauna von Mandschukuo (Hym. Apid.). Mitteilungen der Deutschen entomologischen Gesellschaft 7: 2–10.

Reinig W.F. 1939. Die Evolutionsmechanismen, erläutert an den Hummeln. Verhandlungen der Deutschen zoologischen Gesellschaft (Supplement) 12: 170–206.

Richards O.W. 1928a. Bombus and Volucella in the Himalayas. Entomologist’s Monthly Magazine 64: 107–108.

Richards O.W. 1928b. On a collection of humble-bees (Hymenoptera, Bombidae) made in Ladakh by Col. R. Meinertzhagen. Annals and Magazine of Natural History Series 10 2: 333–336. https://doi.org/10.1080/00222932808672888

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

Richards O.W. 1968. The subgeneric divisions of the genus Bombus Latreille (Hymenoptera: Apidae). Bulletin of the British Museum (Natural History) (Entomology) 22: 209–276. https://doi.org/10.5962/bhl.part.9953

Ronquist F. 1996. DIVA 1.1 User's Manual. Computer program and manual available by anonymous FTP from Uppsala University. Available from ftp.uu.se or ftp.systbot.uu.se [accessed 7 Sep. 2020].

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

Saini M.S., Raina R.H. & Ghator H.S. 2015. Indian Bumblebees. B. Singh and M. P. Singh, Dehra Dun, India.

Sandhouse G.A. 1943. The type species of the genera and subgenera of bees. Proceedings of the United States National Museum 92: 519–619. https://doi.org/10.5479/si.00963801.3156.519

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

Schluter D. & Pennell M.W. 2017. Speciation gradients and the distribution of biodiversity. Nature 546: 48–55. https://doi.org/10.1038/nature22897

Schmidt B.C. & Sperling F.A.H. 2008. Widespread decoupling of mtDNA variation and species integrity in Grammia tiger moths (Lepidoptera: Noctuidae). Systematic Entomology 33: 613–634. https://doi.org/10.1111/j.1365-3113.2008.00433.x

Schmidt S., Schmid-Egger C., Mornière 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: 985–1000. https://doi.org/10.1111/1755-0998.12363

Schmiedeknecht H.L.O. 1878. Monographie der in Thüringen vorkommenden Arten der Hymenopteren-Gattung Bombus mit einer allgemeinen Einleitung in dieses Genus. Jenaische Zeitschrift für Naturwissenschaft 12: 303–430.

Skorikov A.S. 1910a. [New forms of bumblebees] (Hymenoptera, Bombidae). ([Preliminary diagnoses]). III. Russkoe éntomologicheskoe Obozrênie 9 (1909): 409–413. [In Russian.]

Skorikov A.S. 1910b. Revision der in der Sammlung des weil. Prof. E. A. Eversmann befindlichen Hummeln. Trudy Russkago éntomologicheskago obshchestva 39: 570–584.

Skorikov A.S. 1914a. Les formes nouvelles des bourdons (Hymenoptera, Bombidae). VI. Russkoe éntomologicheskoe Obozrênie 14: 119–129.

Skorikov A.S. 1914b. Subterraneobombus fedtschenkoi (F. Mor.), un bourdon de Turkestan peu connu (Hymenoptera, Bombidae). Russkoe éntomologicheskoe Obozrênie 14: 287–292.

Skorikov A.S. 1923. [Palaearctic bumblebees. Part I. General biology (including zoogeography)]. Izvestiya Severnoi oblastnoi stantsii zashchity rastenii ot vreditelei 4 (1922): 1–160.

Skorikov A.S. 1931. Die Hummelfauna Turkestans und ihre Beziehungen zur zentralasiatischen Fauna (Hymenoptera, Bombidae). In: Lindholm V.A. (ed.) Abhandlungen der Pamir-Expedition 1928: 175–247. Academy of Sciences of the USSR, Leningrad.

Skorikov A.S. 1933a. Zur Fauna und Zoogeographie der Hummeln des Himalaya. Doklady Akademii nauk SSSR 1933: 243–248.

Skorikov A.S. 1933b. Zur Hummelfauna Japans und seiner Nachbarländer. Mushi 6: 53–65.

Smith F. 1852a. Descriptions of some hymenopterous insects from northern India. Transactions of the Entomological Society of London 7 (2): 45–48. https://doi.org/10.1111/j.1365-2311.1852.tb02209.x

Smith F. 1852b. Descriptions of some new and apparently undescribed species of hymenopterous insects from north China, collected by Robert Fortune, Esq. Transactions of the Entomological Society of London 7 (2): 33-45. https://doi.org/10.1111/j.1365-2311.1852.tb02208.x

Smith F. 1854. Catalogue of Hymenopterous Insects in the Collection of the British Museum. Part II. Apidae. Trustees of the British Museum, London. https://doi.org/10.5962/bhl.title.20858

Smith F. 1861. Descriptions of new genera and species of exotic Hymenoptera. Journal of Entomology 1: 146–155.

Smith F. 1870. [V. Notes on the habits of some hymenopterous insects from the North-west Provinces of India. By Charles Horne, Esq., B.C.S., F.Z.S.] With an appendix, containing descriptions of some new species of Apidae and Vespidae collected by Mr. Horne: by Frederick Smith, of the British Museum. Illustrated by plates from drawings by the author of the notes. Transactions of the Zoological Society of London 7: 161–196. https://doi.org/10.5962/bhl.title.56718

Starr C.K. 1989. Bombus folsomi and the origin of Philippine bumble bees (Hymenoptera: Apidae). Systematic Entomology 14: 411–415. https://doi.org/10.1111/j.1365-3113.1989.tb00294.x

Starr C.K. 1992. The bumble bees (Hymenoptera: Apidae) of Taiwan. Bulletin of the National Museum of Natural Science 3: 139–157.

Streinzer M., Chakravorty J., Neumayer J., Megu K., Narah J., Schmitt T., Bharti H., Spaethe J. & Brockmann A. 2019. Species composition and elevational distribution of bumble bees (Hymenoptera: Apidae: Bombus) in the East Himalaya, Arunachal Pradesh, India. ZooKeys 851: 71–89. https://doi.org/10.3897/zookeys.851.32956

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. & Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023

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

Tkalců B. 1968. Neue Arten der Unterfamilie Bombinae der paläarktischen Region (Hymenoptera, Apoidea). Sborník Entomologického oddeleni Národního musea v Praze 65: 21–51.

Tkalců B. 1972. Arguments contre l’interprétation traditionelle de la phylogénie des abeilles (Hymenoptera, Apoidea). Première partie, introduction et exposés fondamentaux. Bulletin de la Société entomologique de Mulhouse 1972: 17–28.

Tkalců B. 1974a. Eine Hummel-Ausbeute aus dem Nepal-Himalaya (Insecta, Hymenoptera, Apoidea, Bombinae). Senckenbergiana biologica 55: 311–349.

Tkalců B. 1974b. Ergebnisse der 1. und 2. mongolisch-tschechoslowakischen entomologisch-botanischen Expedition in der Mongolei. Nr. 29: Hymenoptera, Apoidea, Bombinae. Sborník faunistickych prací Entomologického oddelení Národního musea v Praze 15: 25–57.

Tkalců B. 1975. Beitrag zur Kenntnis der Hummelfauna der französischen Basses-Alpes (Hymenoptera, Apoidea, Bombinae). Sborník Slovenského Narodného Muzea 20 (1974): 167–186.

Tkalců B. 1989. Neue Taxa asiatischer Hummeln (Hymenoptera, Apoidea). Acta entomologica bohemoslovaca 86: 39–60.

USBGN 1968. Official Standard Names Gazetteer, No. 13. Indonesia and Portuguese Timor. US Army Topographic Command, Washington D.C.

USBGN 1970. Official Standard Names Gazetteer, No. 10. Malaysia, Singapore, and Brunei. US Army Topographic Command, Washington D.C.

Vieites D.R., Wollenberg K.C., Andreone F., Köhler J., Glaw F. & Vences M. 2009. Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the United States of America 106: 8267–8272. https://doi.org/10.1073/pnas.0810821106

Villers C.J.d. 1789. Caroli Linnæi Entomologia, Faunæ Suecicæ Descriptionibus Aucta; DD. Scopoli, Geoffroy, de Geer, Fabricii, Schrank, &c. speciebus vel in systemate non enumeratis, vel nuperrime detectis, vel speciebus Galliæ australis locupletata, generum specierumque rariorum iconibus ornata; curante & augente Carolo de Villers, Acad. Lugd. Maffil. Villa-Fr. Rhotom. necnon geometriæ regio professore. Vol. 3. Piestre et Delamolliere, Lyon [Lugduni]. https://doi.org/10.5962/bhl.title.12476

Vogt O. 1909. Studien über das Artproblem. 1. Mitteilung. Über das Variieren der Hummeln. 1. Teil. Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin 1909: 28–84.

Vogt O. 1911. Studien über das Artproblem. 2. Mitteilung. Über das Variieren der Hummeln. 2. Teil. (Schluss). Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin 1911: 31–74.

von Dalla Torre K.W. 1890. Hymenopterologische Notizen. Wiener entomologische Zeitung 9: 139.

von Dalla Torre K.W. 1896. Catalogus Hymenopterorum hucusque Descriptorum Systematicus et Synonymicus. Volumen X: Apidae (Anthophila). G. Engelmann, Leipzig [Lipsiae]. https://doi.org/10.5962/bhl.title.10348

Wallace A.R. 1865. On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Transactions of the Linnean Society of London 25: 1–71. https://doi.org/10.5962/bhl.title.9531

Wang S.-F. 1979. Three new species of bomble [sic] bees from Tibet. Acta entomologica sinica 22: 188–191.

Wang S.-F. 1982. Hymenoptera: Apidae - Bombus. In: Qinghai-Tibet Plateau Comprehensive Scientific Investigation Team of the Chinese Academy of Sciences (ed.) Insects of Xizang: 427–447. Science Press, Beijing.

Wang S.-F. 1985. Apidae - Bombus. In: [Organisms of the Tumuefeng region of Tianshan]: 160–165.

Wang S.-F. & Yao J. 1996. Hymenoptera: Apodae [sic] - Bombini. In: Huang F.-S. (ed.) Insects of the Karakorum-Kunlun Mountains: 303–309. Science Press, Beijing.

Wickham H. 2011. GGPLOT2. WIREs Computational Statistics 3: 180–185. https://doi.org/10.1002/wics.147

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 (Natural History) (Entomology) 60: 1–204.

Williams P.H. 1998. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of The Natural History Museum (Entomology) 67: 79–152. Available and updated from www.nhm.ac.uk/bombus/ [accessed 2019].

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. 2011. Bumblebees collected by the Kyushu University Expeditions to Central Asia (Hymenoptera, Apidae, genus Bombus). Esakia 50: 27–36.

Williams P.H. 2018. In a group of its own? Rediscovery of one of the world’s rarest and highest mountain bumblebees, Bombus tanguticus. Journal of Natural History 52: 305–321. https://doi.org/10.1080/00222933.2018.1428377

Williams P.H. submitted. Discriminating true from false cryptic species - is quick also dirty? In: Systematics Association biennual Meeting, Bristol.

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., Tang Y., Yao J. & Cameron S. 2009. The bumblebees of Sichuan (Hymenoptera: Apidae, Bombini). Systematics and Biodiversity 7: 101–190. 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.

Williams P.H., An J.-D. & Huang J.-X. 2011. The bumblebees of the subgenus Subterraneobombus: integrating evidence from morphology and DNA barcodes (Hymenoptera, Apidae, Bombus). Zoological Journal of the Linnean Society 163: 813–862. https://doi.org/10.1111/j.1096-3642.2011.00729.x

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. 2012a. 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., Byvaltsev A.M., Sheffield C.S. & Rasmont P. 2012b. Bombus cullumanus – an extinct European bumblebee species? Apidologie 44: 121–132. https://doi.org/10.1007/s13592-012-0161-x

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, NJ.

Williams P.H., Bystriakova N., Huang J.-X., Miao Z.-Y. & An J.-D. 2015a. Bumblebees, climate and glaciers across the Tibetan plateau (Apidae: Bombus Latreille). Systematics and Biodiversity 13: 164–181. https://doi.org/10.1080/14772000.2014.982228

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. 2015b. Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE 10: 1–26. 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. 2017a. 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 19 Aug. 2020].

Williams P.H., Lobo J.M. & Meseguer A.S. 2017b. Bumblebees take the high road: climatically integrative biogeography shows that escape from Tibet, not Tibetan uplift, is associated with divergences of present-day Mendacibombus. Ecography 41: 461–477. https://doi.org/10.1111/ecog.03074

Williams P.H., Berezin M.V., Cannings S.G., Cederberg B., Ødegaard F., Rasmussen C., Richardson L.L., Rykken J., Sheffield C.S., Thanoosing C. & Byvaltsev A.M. 2019. The arctic and alpine bumblebees of the subgenus Alpinobombus revised from integrative assessment of species’ gene coalescents and morphology (Hymenoptera, Apidae, Bombus). Zootaxa 4625: 1–68. https://doi.org/10.11646/zootaxa.4625.1.1

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

Winter K., Adams L., Thorp R.W., Inouye D.W., Day L., Ascher J. & Buchmann S. 2006. Importation of non-native bumble bees into North America: potential consequences of using Bombus terrestris and other non-native bumble bees for greenhouse crop pollination in Canada, Mexico, and the United States. In: A White Paper of the North American Pollinator Protection Campaign (NAPCC): 33. San Francisco.

Woodard S.H., Lozier J.D., Goulson D., Williams P.H., Strange J. & Jha S. 2015. Molecular tools and bumble bees: revealing hidden details of ecology, evolution, and behavior in a model system. Molecular Ecology 24: 2916–2936. https://doi.org/10.1111/mec.13198

Yasumatsu K. 1935. Insects of Jehol, VIII. Superfamily Apoidea (Order Hymenoptera, II). Art 67. In: Report of the First Scientific Expedition, Manchuoko, Section 5: 1–47.

Yu Y., Blair C. & He X.-J. 2019. RASP 4: ancestral state reconstruction tool for multiple genes and characters. Molecular Biology and Evolution 37: 604–606. https://doi.org/10.1093/molbev/msz257

Zachos J.C., Pagani M., Sloan L., Thomas E. & Billups K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to Present. Science 292: 686–693. https://doi.org/10.1126/science.1059412

Zayed A. & Packer L. 2005. Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences of the United States of America 102: 10742–10746. https://doi.org/10.1073/pnas.0502271102

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

How to Cite
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), 1–120. https://doi.org/10.5852/ejt.2020.719.1107