Bumblebees with big teeth: revising the subgenus Alpigenobombus with the good, the bad and the ugly of numts (Hymenoptera: Apidae)
Abstract
The mountain bumblebees of the subgenus Alpigenobombus Skorikov, 1914, are uniquely distinctive because the females have enlarged mandibles with six large, evenly spaced teeth, which they use to bite holes in long-corolla flowers for nectar robbing. Recognition of species in this subgenus has been uncertain, with names used in various combinations. To revise the species, we examined COI-like barcodes for evidence of species’ gene coalescents using MrBayes and PTP and we compare the coalescent groups with morphological variation for integrative assessment. While we seek to include only orthologous barcodes (the ‘good’) and exclude all of the more strongly divergent barcode-like numts (the ‘bad’), for some nominal taxa only low-divergence numts could be obtained (the ‘ugly’). For taxa with no orthologous sequences available, using a minimum number of the lowest divergence numts did yield coalescent candidates for species that were consistent with morphologically diagnosable groups. These results agree in recognising 11 species within this subgenus, supporting: (1) recognising the widespread European Bombus mastrucatus Gerstaecker, 1869 stat. rev. as a species separate from the west Asian B. wurflenii Radoszkowski, 1860 s. str.; (2) the recently recognised B. rainai Williams, 2022, as a species separate from B. kashmirensis Friese, 1909, within the western Himalaya; (3) the recognition once again of B. sikkimi Friese, 1918 stat. rev. and B. validus Friese, 1905 stat. rev. as species separate from B. nobilis Friese, 1905 s. str. within the eastern Himalaya and Hengduan regions; (4) confirming the recognition of B. angustus Chiu, 1948, B. breviceps Smith, 1852 s. lat., B. genalis Friese, 1918, and B. grahami (Frison, 1933) as separate species within the Himalaya, China, and Southeast Asia; (5) recognising the conspecificity of the nominal taxa (not species) channicus Gribodo, 1892 (Southeast Asia) and dentatus Handlirsch, 1888 (Himalaya) as parts of the species B. breviceps s. lat. (southern and eastern China); and (6) recognising the conspecificity of the rare taxon beresovskii (Skorikov, 1933) syn. n. as part of the species B. grahami within China. Nectar robbing by bumblebees is reviewed briefly and prospects for future research discussed.
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
Anonymous 2001. The Times Comprehensive Atlas of the World. Times Books, London.
Barrowclough G.F. 1982. Geographic variation, predictiveness, and subspecies. Auk 99: 601–603. https://doi.org/10.1007/978-1-4615-6781-3_6
Baum D. & Smith S. 2012. Tree Thinking: An Introduction to Phylogenetic Biology. Roberts and Company, Greenwood Village.
Bensasson D., Zhang D.X., Hartl D.L. & Hewitt G.M. 2001. Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology and Evolution 16: 314–321. https://doi.org/10.1016/S0169-5347(01)02151-6
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.
Brian A.D. 1954. The foraging of bumble bees. Bee World 35: 61–67, 81–91. https://doi.org/10.1080/0005772X.1954.11096671
Brigandt I. & Griffiths P.E. 2007. The importance of homology for biology and philosophy. Biology & Philosophy 22: 633–641. https://doi.org/10.1007/s10539-007-9094-6
Burger F., Creutzburg F., Hartmann J. & Hartmann M. 2009. Die Hummeln von Nepal (Insecta: Hymenoptera: Apidae: Bombus). In: Hartmann M. & Weipert J. (eds) Biodiversität und Naturausstattung im Himalaya III: 455–462. Verein der Freunde und Förderer des Naturkundemuseums Erfurt e.V., Erfurt.
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
Carlini D.B., Chen Y. & Stephan W. 2001. The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. Genetics 159: 623–633. https://doi.org/10.1093/genetics/159.2.623
Chalcoff V.R., Sasal Y., Graham L.E., Vázquez D.P. & Morales C.L. 2022. Invasive bumble bee disrupts a pollination mutualism over space and time. Biological Invasions 24: 1439–1452. https://doi.org/10.1007/s10530-022-02729-2
Chiu S.C. 1948. Revisional notes on the Formosan bombid-fauna (Hymenoptera). Notes d’entomologie chinoise 12: 57–81.
Cockerell T.D.A. 1909. Descriptions and records of bees. – XXIII. Annals and Magazine of Natural History (8) 4: 393–404. https://doi.org/10.1080/00222930908692687
Cockerell T.D.A. 1922. Bees in the collection of the United States National Museum. – 4. Proceedings of the United States National Museum 60: 1–20. https://doi.org/10.5479/si.00963801.60-2413.1
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 11 Aug. 2023].
Darwin C. 1877. The Effects of Cross and Self Fertilisation in the Vegetable Kingdom. D. Appleton, London. https://doi.org/10.5962/bhl.title.104481
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.891.32056
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: 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.
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. BMC Evolutionary Biology 7: 214. https://doi.org/10.1186/1471-2148-7-214
Françoso E., Zuntini A.R., Carnaval A.C. & Arias M.C. 2016. Comparative phylogeography in the Atlantic forest and Brazilian savannas: Pleistocene fluctuations and dispersal shape spatial patterns in two bumblebees. BMC Evolutionary Biology 16: 267. https://doi.org/10.1186/s12862-016-0803-0
Free J.B. 1962. The behaviour of honeybees visiting field beans (Vicia faba). Journal of Animal Ecology 31: 497–502. https://doi.org/10.2307/2049
Free J.B. & Butler C.G. 1959. Bumblebees. New Naturalist Series, Collins, London.
Friese H. 1905. Neue oder wenig bekannte Hummeln des russischen Reiches (Hymenoptera). Ezhegodnik Zoologicheskago muzeya 9: 507–523.
Friese H. 1909. Neue Varietäten von Bombus (Hym.). Deutsche Entomologische Zeitschrift 1909: 673–676. https://doi.org/10.1002/mmnd.48019090519
Friese H. 1911a. Neue Varietäten von Bombus, III. Deutsche Entomologische Zeitschrift 1911: 571–572. https://doi.org/10.1002/mmnd.48019110510
Friese H. 1911b. Zur Synonymie der Bombus-Arten (Hym.). Deutsche Entomologische Zeitschrift 1911: 684. https://doi.org/10.1002/mmnd.48019110611
Friese H. 1916. Über einige neue Hummelformen (Bombus), besonders aus Asien. (Hym.). Deutsche Entomologische Zeitschrift 1916: 107–110. https://doi.org/10.1002/mmnd.48019160205
Friese H. 1918. Über Hummelformen aus dem Himalaja. Deutsche Entomologische Zeitschrift 1918: 81–86.
Friese H. & von Wagner F. 1910. Zoologische Studien an Hummeln. I. Die Hummeln der deutschen Fauna. Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere 29: 1–104. Available from https://www.biodiversitylibrary.org/page/27518513 [accessed 11 Aug. 2023].
Friese H. & von Wagner F. 1912. Zoologische Studien an Hummeln. II. Die Hummeln der Arktis, des Hochgebirges und der Steppe. Zoologische Jahrbücher, Supplement 15: 155–210.
Frison T.H. 1933. Records and descriptions of Bremus and Psithyrus from India (Bremidae: Hymenoptera). Records of the Indian Museum 35: 331–342. https://doi.org/10.26515/rzsi/v35/i3/1933/162591
Frison T.H. 1935. Records, notes and descriptions of Bremus from Asia (Bremidae: Hymenoptera). Records of the Indian Museum 37: 339–363. https://doi.org/10.26515/rzsi/v37/i3/1935/162974
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
Funk W.C. & Omland K.E. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34: 397–423. https://doi.org/10.1146/annurev.ecolsys.34.011802.132421
Gerstaecker A. 1869. Beiträge zur näheren Kenntniss einiger Bienen-Gattungen. Entomologische Zeitung 30: 315–367. Available from https://www.biodiversitylibrary.org/page/9235137 [accessed 11 Aug. 2023].
Goulson D. 2010. Bumblebees, Behaviour, Ecology, and Conservation. 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. Available from https://www.biodiversitylibrary.org/page/16348662 [accessed 11 Aug. 2023].
Hagen E.v. & Aichhorn A. 2003. Hummeln: Bestimmen, Ansiedeln, Vermehren, Schützen. Fauna-Verlag, Nottuln.
Handlirsch A. 1888. Die Hummelsammlung des k. k. naturhistorischen Hofmuseums. Annalen des K.K. Naturhistorischen Hofmuseums 3: 209–250. Available from https://www.biodiversitylibrary.org/page/5749706 [accessed 11 Aug. 2023].
Harder L.D. 1983. Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57: 274–280. https://doi.org/10.1007/BF00379591
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 101: 14812–14817. https://doi.org/10.1073/pnas.0406166101
Heinrich B. 1976. Bumblebee foraging and the economics of sociality. American Scientist 64: 384–395.
Heinrich B. 1979. Bumblebee Economics. Harvard University Press, Cambridge, MA
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
Huang S.-F. 2011. Historical biogeography of the flora of Taiwan. Journal of the National Taiwan Museum 64: 33–63.
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. Fourth Edition. International Commission on Zoological Nomenclature, London. Available from https://www.iczn.org/the-code/the-code-online/ [accessed 13 Aug. 2023].
Inouye D.W. 1980. The terminology of floral larceny. Ecology 61: 1251–1253. https://doi.org/10.2307/1936841
Irwin R.E., Bronstein J.L., Manson J.S. & Richardson L. 2010. Nectar robbing: ecological and evolutionary perspectives. Annual Review of Ecology, Evolution, and Systematics 41: 271–292. https://doi.org/10.1146/annurev.ecolsys.110308.120330
Iserbyt S., Durieux E.-A. & Rasmont P. 2008. The remarkable diversity of bumblebees (Hymenoptera: Apidae: Bombus) in the Eyne Valley (France, Pyrénées-Orientales). Annales de la Société entomologique de France 44: 211–241. https://doi.org/10.1080/00379271.2008.10697558
Krüger E. 1917. Zur Systematik der mitteleuropäischen Hummeln (Hym.). Entomologische Mitteilungen 6: 55–66. Available from https://www.biodiversitylibrary.org/page/10187013 [accessed 13 Aug. 2023].
Kugler H. 1943. Hummeln als Blütenbesucher. Ergebnisse der Biologie 19: 143–323.
Kupyanskaya A.N. 1995. [Family Apidae]. In: Lehr P.A. (ed.) [Key to Insects of the Russian Far East]: 551–580. St Petersburg. [In Russian.]
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
Leadbeater E. & Chittka L. 2008. Social transmission of nectar-robbing behaviour in bumblebees. Proceedings of the Royal Society of London (B) 275: 1669–1674. https://doi.org/10.1098/rspb.2008.0270
Leite L.A.R. 2012. Mitochondrial pseudogenes in insect DNA barcoding: differing points of view on the same issue. Biota Neotropica 12: 301–308. https://doi.org/10.1590/S1676-06032012000300029
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]. Histoire naturelle des Insectes. Hyménoptères. Librairie Encyclopédique de Roret, Paris (1836). https://doi.org/10.5962/t.173542
Løken A. 1949. Bumble bees in relation to Aconitum septentrionale in Central Norway (Oeyer). Nytt Magasin for Naturvidenskapene 87: 1–60.
Løken A. 1950. Bumble bees in relation to Aconitum septentrionale in Western Norway (Eidfjord). Norsk entomologisk Tidsskrift 8: 1–16.
Løken A. 1973. Studies on Scandinavian bumble bees (Hymenoptera, Apidae). Norsk entomologisk Tidsskrift 20: 1–218.
Lopez J.V., Yuhki N., Masuda R., Modi W. & O’Brien S.J. 1994. Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution 39: 174–190. https://doi.org/10.1007/BF00163806
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
Matsuura M. & Yamane S. 1990. Biology of the Vespine Wasps. Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-75230-8
Matzke N.J. 2013a. BioGeoBEARS: bioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts, R package, version 0.2.1, published July 27, 2013. Available from http://CRAN.R-project.org/package=BioGeoBEARS [accessed 13 Aug. 2023].
Matzke N.J. 2013b. 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
Matzke N.J. 2014. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63: 951–970. https://doi.org/10.1093/sysbio/syu056
Mayo S.J. 2022. Cryptic species – a product of the paradigm difference between taxonomic and evolutionary species. In: Monro A.K. & Mayo S.J. (eds) Cryptic Species: Morphological Stasis, Circumscription, and Hidden Diversity: 14–35. Cambridge University Press, Bristol. https://doi.org/10.1017/9781009070553.002
Michener C.D. 2000. The Bees of the World. John Hopkins University Press, Baltimore.
Milliron H.E. 1961. Revised classification of the bumblebees – a synopsis (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 34: 49–61.
Morawitz F.F. 1874. Die Bienen Daghestans. Trudy Russkago éntomologicheskago obshchestva 10: 129–189.
Morawitz F.F. 1880. Ein Beitrag zur Bienen-Fauna mittel-Asiens. Izvêstiya Imperatorskoi akademii nauk 26: 337–379.
Moulton M.J., Song H. & Whiting M.F. 2010. Assessing the effects of primer specificity on eliminating numt coamplification in DNA barcoding: a case study from Orthoptera (Arthropoda: Insecta). Molecular Ecology Resources 10: 615–627. https://doi.org/10.1111/j.1755-0998.2009.02823.x
Neumayer J. 1998. Habitatpräferenzum alpiner Hummelarten (Hymenoptera, Apidae, Bombus, Psithyrus): Meereshöhe und Lage im Gebirgsrelief als Faktoren der Nischentrennung. Wissenschaftliche Mitteilungen aus dem Nationalpark Hohe Tauern 4: 159–174.
Neumayer J. & Paulus H.F. 1999. Ökologie alpiner Hummelgemeinschaften: Blütenbesuch, Ressourcenaufteilung und Energiehaushalt. Untersuchungen in den Ostalpen Österreichs. Biologiezentrum des Oberösterreichischen Landesmuseums, Linz.
Ollerton J. 2020. Pollinators & Pollination: Nature and Society. Pelagic Publishing Exeter. https://doi.org/10.53061/JAOK9895
Ornosa C. & Ortiz-Sanchez F.J. 2004. Hymenoptera Apoidea I. In: Sánchez M.A. et al. (eds) Fauna Iberica, Vol. 23. Museo Nacional de Ciencias Naturales, Madrid.
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
Pekkarinen A. 1979. Morphometric, colour and enzyme variation in bumblebees (Hymenoptera, Apidae, Bombus) in Fennoscandia and Denmark. Acta zoologica Fennica 158: 1–60.
Pérez J. 1890a. Catalogue des mellifères du sud-ouest. Actes de la Société linnéenne de Bordeaux 44: 133–200. Available from https://www.biodiversitylibrary.org/page/27383562 [accessed 13 Aug. 2023].
Pérez J. 1890b. Sur la faune apidologique du sud-ouest de la France. Compte Rendu de la Association Francaise pour l’Avancement des Sciences 111: 991–993.
Pesenko Y.A. & Astafurova Y.V. 2003. Annotated bibliography of Russian and Soviet publications on the bees (Hymenoptera: Apoidea; excluding Apis mellifera): 1771–2003. Denisia 11: 1–616.
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. 1937. Die Hummelfauna des Kalsbachtales in Ost-Tirol. Ein Beitrag zur Ökologie und Systematik der Hummeln Mitteleuropas. Festschrift zum 60. Geburtstag von Professor Dr Embrik Strand 3: 64–122.
Pittioni B. 1938. Die Hummeln und Schmarotzerhummeln der Balkan-Halbinsel. Mit besonderer Berücksichtigung der Fauna Bulgariens. I. Allgemeiner Teil. Izvestiya na Tsarskite prirodonauchni instituti v Sofiya 11: 2–69.
Pittioni B. 1939. Die Hummeln und Schmarotzerhummeln der Balkan-Halbinsel. II. Spezieller Teil. Izvestiya na Tsarskite prirodonauchni instituti v Sofiya 12: 49–115.
Pyke G.H. 1982. Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community structure. Ecology 63: 555–573. https://doi.org/10.2307/1938970
R_Core_Team 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/ [accessed 13 Aug. 2032].
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. Essai d’une nouvelle méthode pour faciliter la détermination des espèces appartenant au genre Bombus. Byulleten’ Moskovskogo obshchestva ispytatelei prirody 52: 169–219.
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. & Flagothier D. 1996. Biogéographie et choix floraux des bourdons (Hymenoptera, Apidae) de la Turquie. Rapport préliminaire 1995–1996 NATO–OTAN TU-Pollination Project. Université de Mons-Hainaut, Mons, Belgium.
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 (www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. https://doi.org/10.1111/j.1471-8286.2006.01678.x
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. 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. & Rasmont P. 1988. Beitrag zur Kenntnis des Bergwaldhummel Alpigenobombus wurfleini [sic] (Radoszkowski, 1859) (Hymenoptera, Apidae, Bombinae). Spixiana 11: 37–67. Available from https://www.biodiversitylibrary.org/page/28193893 [accessed 13 Aug. 2023].
Ricardo P.C. 2017. Heteroplasmy in Bombus morio (Hymenoptera, Apidae) and Impacts in Evolutionary Studies. Master Dissertation, Universidade de Sao Paulo. https://doi.org/10.11606/D.41.2018.tde-02042018-150706
Richards O.W. 1928. On a collection of humble-bees (Hymenoptera, Bombidae) made in Ladakh by Col. R. Meinertzhagen. Annals and Magazine of Natural History (10) 2: 333–336. https://doi.org/10.1080/00222932808672888
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
Richardson S.C. 2004. Are nectar-robbers mutualists or antagonists? Oecologia 139: 246–254. https://doi.org/10.1007/s00442-004-1504-8
Ronquist F. 1996. DIVA 1.1 User’s Manual. Available from ftp.uu.se or ftp.systbot.uu.se [accessed 13 Aug. 2023)
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
Rosenberger N.M., Aizen M.A., Dickson R.G. & Harder L.D. 2021. Behavioural responses by a bumble bee to competition with a niche-constructing congener. Journal of Animal Ecology 91: 580–592. https://doi.org/10.1111/1365-2656.13646
Sahel N. & Chittka L. 2007. Traplining in bumblebees (Bombus impatiens): a foraging strategy’s ontogeny and the importance of spatial reference memory in short-range foraging. Oecologia 151: 719–730. https://doi.org/10.1007/s00442-006-0607-9
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/10.116/annurev-ento-112408-085432
Scopoli J.A. 1763. Entomologia Carniolica exhibens insecta Carnioliæ indigena et distributa in ordines, genera, species, varietates. Typis Ioannis Thomae Trattner, Vienna [Vindobonae]. https://doi.org/10.5962/bhl.title.34434
Simpson G.G. 1940. Types in modern taxonomy. American Journal of Science 238: 413–431. https://doi.org/10.2475/ajs.238.6.413
Skorikov A.S. 1910. [A contribution to the fauna and geographical distribution of bumblebees (Bombus) in northern Caucasus (a preliminary report)]. Trudy Obshchestva Ispytatelei Prirody pri Imperatorskom Khar'kovskom Universitete (Kharkov) 43 (1909): 77–84. [In Russian.]
Skorikov A.S. 1914. Les formes nouvelles des bourdons (Hymenoptera, Bombidae). VI. Russkoe éntomologicheskoe Obozrênie 14: 119–129.
Skorikov A.S. 1923. [Palaearctic bumblebees. Part I. General biology (including zoogeography)]. Izvestiya Severnoi oblastnoi stantsii zashchity rastenii ot vreditelei 4 (1922): 1–160. [In Russian.]
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. 1852. 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 2: 33–45. https://doi.org/10.1111/j.1365-2311.1852.tb02208.x
Song H., Buhay J.E., Whiting M.F. & Crandall K.A. 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105: 13486–13491. https://doi.org/10.1073/pnas.0803076105
Song H., Moulton M.J. & Whiting M.F. 2014. Rampant nuclear insertion of mtDNA across diverse lineages within Orthoptera (Insecta). PLoS ONE 9: e110508. https://doi.org/10.1371/journal.pone.0110508
Soper M.H.R. 1952. A study of the principal factors affecting the establishment and development of the field bean (Vicia faba). Journal of agricultural Science 42: 335–346. https://doi.org/10.1017/S0021859600057233
Starr C.K. 1992. The bumble bees (Hymenoptera: Apidae) of Taiwan. Bulletin of the National Museum of Natural Science 3: 139–157.
Strand E. 1901. Orthoptera og Hymenoptera samlede i 1900. Archiv for Mathematik og Naturvidenskab 23: 1–7. Available from https://www.biodiversitylibrary.org/page/30015041 [accessed 13 Aug. 2023].
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
Sun C., Huang J.-X., Wang Y., Zhao X.-M., Su L., Thomas G.W.C., Zhao M.-Y., Zhang X.-T., Jungreiss I., Kellis M., Vicario S., Sharakov I.V., Bondarenko S., Hasselmann M., Kim C.N., Paten B., Penso-Dolfin L., Wang L., Chang Y.-X., Gao Q., Ma L., Ma L., Zhang Z., Zhang H.-H., Ruzzante L., Robertson H.M., Zhu Y.-H., Liu Y.-J., Yang H.-P., Ding L., Wang Q.-G., Xu W.-L., Liang C., Itgen M.W., Mee L., Sadd B.M., Cao G., Zhang Z., Hahn M.W., Schaack S., Barribeau S.M., Williams P.H., Waterhouse R.M. & Mueller R.L. 2020. Genus-wide characterization of bumblebee genomes reveals variation associated with key ecological and behavioral traits of pollinators. Molecular Biology and Evolution 38: 486–501. https://doi.org/10.1093/molbev/msaa240
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
Talavera G., Lukhtanov V., Pierce N.E. & Vila R. 2021. DNA barcodes combined with multilocus data of representative taxa can generate reliable higher-level phylogenies. Systematic Biology 71: 382–395. https://doi.org/10.1093/sysbio/syab038
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://academic.oup.com/mbe/article/30/12/2725/1017851
Thanoosing C. 2022. Systematics and Ecology of Southeast Asian Bumblebees. Imperial College London, London.
Thomson C.G. 1870. Oefversigt af Sveriges humlor. Opuscula Entomologica 2: 251–261. Available from https://www.biodiversitylibrary.org/page/10170441 [accessed 13 Aug. 2023].
Tkalců B. 1968. Revision der vier sympatrischen, homochrome geographische Rassen bildenden Hummelarten SO-Asiens (Hymenoptera, Apoidea, Bombinae). Annotationes Zoologicae et Botanicae 52: 1–31.
Tkalců B. 1969. Ergebnisse der Albanien-Expedition 1961 des Deutschen Entomologischen Institutes. 78. Beitrag. Hymenoptera: Apidae IV (Bombinae). Beiträge zur Entomologie 19: 887–916.
Tkalců B. 1974. Eine Hummel-Ausbeute aus dem Nepal-Himalaya (Insecta, Hymenoptera, Apoidea, Bombinae). Senckenbergiana biologica 55: 311–349.
Tkalců B. 1977. Taxonomisches zu einigen paläarktischen Bienenarten (Hymenoptera: Apoidea). Vestník Ceskoslovenské spolecnosti zoologické 41: 223–239.
Tkalců B. 1987. Nouveaux synonymes chez les Bombinae (Hymenoptera, Apoidea). Bulletin de la Société entomologique de Mulhouse 1987: 59–64.
Trunz V., Packer L., Vieu J., Arrigo N. & Praz C.J. 2016. Comprehensive phylogeny, biogeography and new classification of the diverse bee tribe Megachilini: Can we use DNA barcodes in phylogenies of large genera? Molecular Phylogenetics and Evolution 103: 245–259. https://doi.org/10.1016/j.ympev.2016.07.004
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. Available from https://www.biodiversitylibrary.org/page/10332454 [accessed 13 Aug. 2023].
von Dalla Torre K.W. 1896. Catalogus Hymenopterorum hucusque descriptorum systematicus et synonymicus. Vol. X: Apidae (Anthophila). G. Engelmann, Leipzig [Lipsiae]. https://doi.org/10.5962/bhl.title.10348
Wang S.-F. 1979. Three new species of bomble [sic] bees from Tibet. Acta Entomologica Sinica 22: 188–191.
Wang S.-F. 1992. Hymenoptera: Apoidae (II) – Bombus. The Series of the Scientific Expedition to the Hengduan Mountains Region of Qinghai-Xizang Plateau Vol. 1: 1422–1430. Chinese Academy of Sciences.
Wang S.-F. & Yao J. 1993. Studies of the subgenus Alpigenobombus Skorikov of China (Hymenoptera: Apidae). Sinozoologia 10: 415–424.
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. Available from https://www.biodiversitylibrary.org/page/41055963 [accessed 13 Aug. 2023].
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 Natural History Museum (Entomology) 67: 79–152 Available from https://www.biodiversitylibrary.org/page/40885412 [accessed 13 Aug. 2023]. Updated at www.nhm.ac.uk/bombus/ [accessed 2015].
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. 2022a. The Bumblebees of the Himalaya. Abc Taxa 21. Royal Belgian Institute of Natural Sciences, Brussels. Available from http://www.abctaxa.be [accessed 13 Aug. 2023].
Williams P.H. 2022b. Guerrilla taxonomy and discriminating cryptic species - is quick also dirty? In: Monro A.K. & Mayo S.J. (eds) Cryptic Species: Morphological Stasis, Circumscription, and Hidden Diversity: 213–241. Cambridge University Press, Bristol, https://doi.org/10.1017/9781009070553.009
Williams P.H. 2022c. IUCN Bumblebee Sub Group Annual Report 2021. Natural History Museum, London. https://doi.org/10.13140/RG.2.2.18285.46561
Williams P.H. 2022d. Novel splitting/lumping index reflects the history of species concepts applied to bumblebees (Insecta, Apidae). Zoological Journal of the Linnean Society 196: 704–719. https://doi.org/10.1093/zoolinnean/zlab123
Williams P.H. & Jepsen S. 2014. IUCN BBSG – Bumblebee Specialist Group Report 2013. Natural History Museum, London.
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. Available from http://hdl.handle.net/2115/44628 [accessed 13 Aug. 2023].
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. 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., 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: 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 13 Aug. 2023].
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
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., Francoso E., Martinet B., Orr M.C., Ren Z.-X., Santos Junior J., Thanoosing C. & Vandame R. 2022a. When did bumblebees reach South America? Unexpectedly old montane species may be explained by Mexican stopover (Hymenoptera: Apidae). Systematics and Biodiversity 20: 1–24. https://doi.org/10.1080/14772000.2022.2092229
Williams P.H., Sung I.-H., Lin Y.-J. & Lu S.-S. 2022b. Discovering endemic species among the bumblebees of Taiwan (Apidae, genus Bombus). Journal of Natural History 56: 437–447. 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
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. A White Paper of the North American Pollinator Protection Campaign (NAPCC), San Francisco.
Yu Y., Harris A.J. & He X.-J. 2014. RASP (Reconstruct Ancestral State in Phylogenies) 3.0. Available from http://mnh.scu.edu.cn/soft/blog/RASP [accessed 13 Aug. 2023].
Yu Y., Blair C. & He X.-J. 2020. 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
Zhang D.-X. & Hewitt G.M. 1996. Nuclear integrations: challenge for mitochondrial DNA markers. Trends in Ecology and Evolution 11: 247–251. https://doi.org/10.1016/0169-5347(96)10031-8
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
Zimmerman M. & Cook S. 1985. Pollinator foraging, experimental necatr-robbing and plant fitness in Impatiens capensis. American Midlands Naturalist 113: 84–91. https://doi.org/10.2307/2425350
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) 2023 Paul H. Williams, Jiandong An, Phurpa Dorji, Jiaxing Huang, Saleem Jaffar, George Japoshvili, Jaya Narah, Zongxin Ren, Martin Streinzer, Chawatat Thanoosing, Li Tian, Michael C. Orr
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