Following the cold: geographical differentiation between interglacial refugia and speciation in the arcto-alpine species complex Bombus monticola (Hymenoptera: Apidae)
Martinet, Baptiste; Lecocq, Thomas; Brasero Et Martin, Nicolaset al.
2018 • In Systematic Entomology, 43 (1), p. 200-217
[en] Cold-adapted species are expected to have reached their largest distribution
range during a part of the Ice Ages whereas postglacial warming has led to their range
contracting toward high-latitude and high-altitude areas. This has resulted in an extant
allopatric distribution of populations and possibly to trait differentiations (selected or
not) or even speciation. Assessing inter-refugium differentiation or speciation remains
challenging for such organisms because of sampling difficulties (several allopatric
populations) and disagreements on species concept. In the present study, we assessed
postglacial inter-refugia differentiation and potential speciation among populations of
one of the most common arcto-alpine bumblebee species in European mountains,
Bombus monticola Smith, 1849. Based on mitochondrial DNA/nuclear DNA markers
and eco-chemical traits, we performed integrative taxonomic analysis to evaluate
alternative species delimitation hypotheses and to assess geographical differentiation
between interglacial refugia and speciation in arcto-alpine species. Our results show
that trait differentiations occurred between most Southern European mountains (i.e.
Alps, Balkan, Pyrenees, and Apennines) and Arctic regions. We suggest that the
monticola complex actually includes three species: B. konradini stat.n. status distributed
in Italy (Central Apennine mountains), B. monticola with five subspecies, including
B. monticola mathildis ssp.n. distributed in the North Apennine mountains ; and
B. lapponicus. Our results support the hypothesis that post-Ice Age periods can lead to
speciation in cold-adapted species through distribution range contraction. We underline
the importance of an integrative taxonomic approach for rigorous species delimitation,
and for evolutionary study and conservation of taxonomically challenging taxa.
Michez, Denis ; Université de Mons > Faculté des Sciences > Zoologie
Rasmont, Pierre ; Université de Mons > Faculté des Sciences > Service de Zoologie
Language :
English
Title :
Following the cold: geographical differentiation between interglacial refugia and speciation in the arcto-alpine species complex Bombus monticola (Hymenoptera: Apidae)
Andriollo, T., Naciri, Y. & Ruedi, M. (2015) Two mitochondrial barcodes for one biological species: the case of European Kuhl's Pipistrelles (Chiroptera). PLoS ONE, 10, e0134881.
Avise, J.C. (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachusetts.
Ayasse, M. & Jarau, S. (2014) Chemical ecology of bumble bees. Annual Review of Entomology, 59, 299–319.
Ayasse, M., Paxton, R.J. & Tengö, J. (2001) Mating behavior and chemical communication in the order Hymenoptera. Annual Review of Entomology, 46, 31–78.
Baer, B. (2003) Bumblebees as model organisms to study male sexual selection in social insects. Behavioral Ecology and Sociobiology, 54, 521–533.
Barnes, I., Shapiro, B., Lister, A., Kuznetsova, T., Sher, A., Guthrie, D. & Thomas, M.G. (2007) Genetic structure and extinction of the woolly mammoth, Mammuthus primigenius. Current Biology, 17, 1072–1075.
Barraclough, T.G., Birky, C.W. Jr & Burt, A. (2003) Diversification in sexual and asexual organisms. Evolution (N. Y.), 57, 2166–2172.
Bensasson, D., Zhang, D., Hartl, D.L. & Hewitt, G.M. (2001) Mitochondrial Pseudogenes: evolution's miplaced witnesses. Trends in Ecology and Evolution, 16, 314–321.
Bertsch, A. & Schweer, H. (2012a) Cephalic labial gland secretions of males as species recognition signals in bumblebees: are there really geographical variations in the secretions of the Bombus terrestris subspecies? Beiträge zur Entomologie, 62, 103–124.
Bertsch, A. & Schweer, H. (2012b) Male labial gland secretions as species recognition signals in species of Bombus. Biochemical Systematics and Ecology, 40, 103–111.
Braby, M.F., Eastwood, R. & Murray, N. (2012) The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society, 106, 699–716.
Brasero, N., Martinet, B., Urbanová, K. et al. (2015) First chemical analysis and characterization of the male species-specific cephalic labial gland secretions of South American bumblebee. Chemistry & Biodiversity, 12, 1535–1546.
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.
Carolan, J.C., Murray, T.E., Fitzpatrick, U. et al. (2012) Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS ONE, 7, e29251.
Canestrelli, D., Cimmaruta, R. & Nascetti, G. (2008) Population genetic structure and diversity of the Apennine endemic stream frog, Rana italica - insights on the Pleistocene evolutionary history of the Italian peninsular biota. Molecular Ecology, 17, 3856–3872.
Canestrelli, D., Sacco, F. & Nascetti, G. (2012) On glacial refugia, genetic diversity, and microevolutionary processes: deep phylogeographical structure in the endemic newt Lissotriton italicus. Biological Journal of the Linnean Society, 105, 42–55.
Claudet, J., Pelletier, D., Jouvenel, J.Y., Bachet, F. & Galzin, R. (2006) Assessing the effects of marine protected area (MPA) on a reef fish assemblage in a northwestern Mediterranean marine reserve: identifying community-based indicators. Biological Conservation, 130, 346–369.
Conti, F., Abbate, G., Alessandrini, A., Blasi, C., Bonacquisti, S. & Scassellati, E. (2005) An Annotated Checklist of the Italian Vascular Flora. Palombi, Rome.
Coppée, A., Terzo, M., Valterova, I. & Rasmont, P. (2008) Intraspecific variation of the cephalic labial gland secretions in Bombus terrestris (L.) (Hymenoptera: Apidae). Chemistry & Biodiversity, 5, 2654–2661.
Crowhurst, R.S., Faries, K.M., Collantes, J., Briggler, J.T., Koppelman, J.B. & Eggert, L.S. (2011) Genetic relationships of hellbenders in the Ozark highlands of Missouri and conservation implications for the Ozark subspecies (Cryptobranchus alleganiensis bishopi). Conservation Genetics, 12, 637–646.
De Meulemeester, T., Gerbaux, P., Boulvin, M., Coppee, A. & Rasmont, P. (2011) A simplified protocol for bumble bee species identification by cephalic secretion analysis. Insectes Sociaux, 58, 227–236.
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
Dellicour, S. & Lecocq, T. (2013a) GCALIGNER 1.0 and GCKOVATS 1.0 – Manual of a Software Suite to Compute a Multiple Sample Comparison Data Matrix from Eco-chemical Datasets Obtained by Gas Chromatography. University of Mons, Mons.
Dellicour, S. & Lecocq, T. (2013b) GCALIGNER 1.0: an alignment program to compute a multiple sample comparison data matrix from large eco-chemical datasets obtained by GC. Journal of Separation Science, 36, 3206–3209.
Dellicour, S., Lecocq, T., Kuhlmann, M., Mardulyn, P. & Michez, D. (2014a) Molecular phylogeny, biogeography, and host plant shifts in the bee genus Melitta (Hymenoptera: Anthophila). Molecular Phylogenetics and Evolution, 70, 412–419.
Dellicour, S., Fearnley, S., Lombal, A., Heidl, S., Dahlhoff, E.P., Rank, N.E. & Mardulyn, P. (2014b) Inferring the past and present connectivity across the range of a North American leaf beetle: combining ecological niche modeling and a geographically explicit model of coalescence. Evolution, 68, 2371–2385.
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.
Dellicour, S., Kastally, C., Varela, S., Michez, D., Rasmont, P., Mardulyn, P. & Lecocq, T. (2016) Ecological niche modelling and coalescent simulations to explore the recent geographic range history of five widespread bumblebee species in Europe. Journal of Biogeography, 44, 39–50. https://doi.org/10.1111/jbi.12748.
Dufrene, M. & Legendre, P. (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67, 345–366.
Ebach, M.C. & Williams, D.M. (2009) How objective is a definition in the subspecies debate? Nature, 457, 785.
Ennen, J.R., Kalis, M.E., Patterson, A.L., Kreiser, B.R., Lovich, J.E., Godwin, J. & Qualls, C.P. (2014) Clinal variation or validation of a subspecies? A case study of the Graptemys nigrinoda complex (Testudines: Emydidae). Biological Journal of the Linnean Society, 111, 810–822.
Evans, R.L. & Potts, S.G. (2013) Iconic Bees: North East Bilberry Bumblebee. Friends of the Earth. University of Reading, Reading.
Fedorov, V.B., Goropashnaya, A.V., Boeskorov, G.G. & Cook, J.A. (2008) Comparative phylogeography and demographic history of the wood lemming (Myopus schisticolor): implications for late Quaternary history of the taiga species in Eurasia. Molecular Ecology, 17, 598–610.
Fitzpatrick, U., Murray, T.E., Paxton, R.J. & Brown, M.J.F. (2006) The State of Ireland's Bees. Northern Ireland Environment Agency Dublin, Republic of Ireland. URL http://www.biodiversityireland.ie/projects/irish-pollinator-initiative/bees/the-state-of-irelands-bees/ [accessed on 15 November 2016].
Frankham, R., Ballou, J.D. & Briscoe, D.A. (2010) Introduction to Conservation Genetics, 644 p., 2nd edn. Cambridge University Press, Cambridge, U.K.
Frattaroli, A.R., Di Martino, L., Di Cecco, V., Catoni, R., Varone, L., Di Santo, M. & Gratani, L. (2013) Seed germination capability of four endemic species in the Central Apennines (Italy): relationships with seed size. Lazaroa, 34, 43–53.
Fritz, U., Fattizzo, T., Guicking, D. et al. (2005) A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudines, Emydidae). Zoologica Scripta, 34, 351–371.
Fuente, V., Rufo Nieto, L. & Sánchez-Mata, D. (2011) Sarcocornia hispanica (Chenopodiaceae), a new species from the Iberian Peninsula. Lazaroa, 32, 9–13.
Galtier, N., Gouy, M. & Gautier, C. (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences, 12, 543–548.
Gjershaug, J., Staverløkk, A., Kleven, O. & Ødegaard, F. (2013) Species status of Bombus monticola Smith (Hymenoptera: Apidae) supported by DNA barcoding. Zootaxa, 3716, 431–440.
Hawlitschek, O., Nagy, Z.T. & Glaw, F. (2012) Island evolution and systematic revision of Comoran snakes: why and when subspecies still make sense. PLoS ONE, 7, e42970.
Hewitt, G. (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87–112.
Hewitt, G.M. (2004a) The structure of biodiversity – Insights from molecular phylogeography. Frontiers in Zoology, 1, 4.
Hewitt, G.M. (2004b) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B, 359, 183–195.
Hewitt, G.M. (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica, 139, 617–638.
Hewitt, G. & Ibrahim, K. (2001) Inferring glacial refugia and historical immigrations with molecular phylogenies. In: Integrating Ecology and Evolution in a Spatial Context (eds J. Silvertown & J. Antonovics), pp. 271–294. Blackwells, Oxford, U.K.
Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.
Hines, H.M. (2008) Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology, 57, 58–75.
Iserbyt, S. & Rasmont, P. (2012) The effect of climatic variation on abundance and diversity of bumblebees: a ten years survey in a mountain hotspot. Annales de la Société entomologique de France (N.S.), 48, 261–273.
Joger, U., Fritz, U., Guicking, D. et al. (2007) Phylogeography of Western palaractic reptiles - Spatial and temporal speciation patterns. Zoologischer Anzeiger, 246, 293–313.
Kraus, F.B., Wolf, S. & Moritz, R.F.A. (2009) Male flight distance and population substructure in the bumblebee Bombus terrestris. Journal of Animal Ecology, 78, 247–252.
Kuhlmann, M., Ascher, J.S., Dathe, H.H. et al. (2014) Checklist of the Western Palaearctic Bees (Hymenoptera: Apoidea: Anthophila) [WWW document]. URL http://westpalbees.myspecies.info. [accessed on 4 November 2015].
Lecocq, T., Lhomme, P., Michez, D., Dellicour, S., Valterova, I. & Rasmont, P. (2011) Molecular and chemical characters to evaluate species status of two cuckoo bumblebees: Bombus barbutellus and Bombus maxillosus (Hymenoptera, Apidae, Bombini). Systematic Entomology, 36, 453–469.
Lecocq, T., Dellicour, S., Michez, D. et al. (2013a) Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BMC Evolutionary Biology, 13, 263.
Lecocq, T., Vereecken, N.J., Michez, D. et al. (2013b) Patterns of genetic and reproductive traits differentiation in mainland vs. Corsican populations of bumblebees. PLoS ONE, 8, e65642.
Lecocq, T., Brasero, N., De Meulemeester, T. et al. (2015a) An integrative taxonomic approach to assess the status of Corsican bumblebees: implications for conservation. Animal Conservation, 18, 236–248.
Lecocq, T., Brasero, N., Martinet, B., Valterovà, I. & Rasmont, P. (2015b) Highly polytypic taxon complex: interspecific and intraspecific integrative taxonomic assessment of the widespread pollinator Bombus pascuorum Scopoli 1763 (Hymenoptera: Apidae). Systematic Entomology, 40, 881–888.
Lecocq, T., Coppee, A., Mathy, T. et al. (2015c) Subspecific differentiation in male reproductive traits and virgin queen preferences, in Bombus terrestris. Apidologie, 46, 595–605.
Lecocq, T., Dellicour, S., Michez, D. et al. (2015d) Methods for species delimitation in bumblebees (Hymenoptera, Apidae, Bombus): towards an integrative approach. Zoologica Scripta, 44, 281–297.
Lecocq, T., Coppée, A., Michez, D., Brasero, N., Rasplus, J.Y., Valterova, I. & Rasmont, P. (2016) The alien's identity: consequences of taxonomic status for the international bumblebee trade regulations. Biological Conservation, 195, 169–176.
Legendre, P. & Legendre, L. (2004) Numerical Ecology, Developments in Environmental Modelling 20, 853p, 2nd edn. Elsevier Scientific Publication Company, Amsterdam, the Netherlands.
Lepais, O., Darvill, B., O'Connor, S. et al. (2010) Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Molecular Ecology, 19, 819–831.
Løken, A. (1973) Studies on Scandinavian bumble bees (Hymenoptera, Apidae). Norsk Entomologisk Tidsskrift, 20, 1–218.
Lunt, D.H., Zhang, D.X., Szymura, J.M. & Hewitt, O.M. (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology, 5, 153–165.
Manino, A., Patetta, A., Porporato, M., Quaranta, M., Intoppa, F., Piazza, M.G. & Friilli, F. (2007) Bumblebee (Bombus Latreille, 1802) distribution in high mountains and global warming. Redia, 90, 125–129.
Mardulyn, P., Mikhailov, Y.E. & Pasteels, J.M. (2009) Testing phylogeographic hypotheses in a euro-siberian cold-adapted leaf beetle with coalescent simulations. Evolution, 63, 2717–2729.
Martín-Bravo, S., Valcárcel, V., Vargas, P. & Luceño, M. (2010) Geographical speciation related to Pleistocene range shifts in the western Mediterranean mountains. Taxon, 59, 466–482.
Martinet, B., Lecocq, T., Smet, J. & Rasmont, P. (2015a) A protocol to assess insect resistance to heat waves, applied to bumblebees (Bombus Latreille, 1802c). PLoS ONE, 10, e0118591.
Mattoccia, M., Marta, S., Romano, A. & Sbordoni, V. (2011) Phylogeography of an Italian endemic salamander (genus Salamandrina): glacial refugia, postglacial expansions, and secondary contact. Biological Journal of the Linnean Society, 104, 903–922.
Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York, New York.
Michener, C.D. (2007) The Bees of the World, 2nd edn. Johns Hopkins University, Baltimore, Maryland.
Mutanen, M., Kivelä, S.M., Vos, R.A. et al. (2016) Species-level Para- and Polyphyly in DNA barcode gene trees: strong operational bias in European Lepidoptera. Systematic Biology, 65, 1025–1040.
Nieto, A., Roberts, S.P.M., Kemp, J. et al. (2014) European Red List of Bees. IUCN, European Commission, Luxembourg.
Oksanen, F.J., Blanchet, G., Kindt, R. et al. (2011) Tertiary Vegan: Community Ecology Package. URL https://cran.r-project.org.
Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.
Patten, M.A. (2009) Subspecies' and ‘race’ should not be used as synonyms. Nature, 457, 147.
Patten, M.A. (2010) Null expectations in subspecies diagnosis. Ornithological Monographs, 67, 35–41.
Patten, M.A. & Unitt, P. (2002) Diagnosability versus mean differences of Sage Sparrow subspecies. The Auk, 119, 26–35.
Pedersen, B.V. (2002) European bumblebees (Hymenoptera: Bombini) – Phylogenetic relationships inferred from DNA sequences. Insect Systematics and Evolution, 33, 361–386.
Petit, R.J., Aguinagalde, I., De Beaulieu, J.L. et al. (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300, 1563–1565.
Phillimore, A.B. & Owens, I.P.F. (2006) Are subspecies useful in evolutionary and conservation biology? Proceedings of the Royal Society of London Series B, 273, 1049–1053.
Posada, D. (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. [WWW document]. URL http://www.R-project.org/ [accessed on 4 November 2015].
Rambaut, A. & Drummond, A.J. (2013) Tracer Version 1.4. [WWW document]. URL http://beast.bio.ed.ac.uk/Tracer [accessed on 15 November 2016].
Rasmont, P. (1983) Catalogue commenté des Bourdons de la région ouest-paléarctique (Hymenoptera, Apoïdea, Apidae). Notes fauniques de Gembloux, 7, 1–72.
Rasmont, P. & Iserbyt, S. (2014) Atlas of the European Bees: genus Bombus, 3rd edn. STEP Project; Status Trends Eur Pollinators, Atlas Hymenoptera, Mons, Gembloux. [WWW document]. URL http://www.zoologie.umh.ac.be//hymenoptera/page.asp?ID=169 [accessed on 15 March 2017].
Rasmont, P., Coppée, A., Michez, D. & De Meulemeester, T. (2008) An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Annales de la Société Entomologique de France (N.S.), 44, 243–250.
Rasmont, P., Franzen, M., Lecocq, T. et al. (2015) Climatic risk and distribution atlas of European bumblebees. BioRisk, 10, 1–236.
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.
Reinig, W.F. (1937) Die Holarktis. Ein Beitrag zur diluvialen und alluvialen Geschichte der Cirkumpolaren Faunen- und Florengebiete. Gustav Fischer, Jena.
Reinig, W.F. (1965) Die Verbreitungsgeschichte zweier fûr die Apenninen neuer boreoalpinen Hummelarten mit einem Versuch der Gliederung boreoalpiner Verbreitungsformen. Jahrbücher Abteilung fur Systernatik, 92, 703–742.
Ricciardelli D' Albore, G. & Piatti, C. (2003) Ecology of Bombus monticola konradini Reinig (Hymenoptera: Apidae) in the National Park of the Sibillini mountains (Central Italy). Annali della Facolta di Agraria, Universita degli Studi di Perugia, 55, 283–291.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Ruiz-Labourdette, D., Nogués-Bravo, D., Sáinz Ollero, H., Schmitz, M.F. & Pineda, F.D. (2012) Forest composition in Mediterranean mountains is projected to shift along the entire elevational gradient under climate change. Journal of Biogeography, 39, 162–176.
Sackett, L.C., Seglund, A., Guralnick, R.P., Mazzella, M.N., Wagner, D.M., Busch, J.D. & Martin, A.P. (2014) Evidence for two subspecies of Gunnison's prairie dogs (Cynomys gunnisoni), and the general importance of the subspecies concept. Biological Conservation, 174, 1–11.
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.
Siegel, S. & Castellan, N.J. (1988) Non Parametric Statistics for the Behavioural Sciences. MacGraw Hill Humanities, New York, New York.
Stewart, J.R., Lister, A.M., Barnes, I. & Dalén, L. (2010) Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society of London Series B, 277, 661–671.
Suzuki, R. & Shimodaira, H. (2011) Pvclust: Hierarchical Clustering with P-values via Multiscale Bootstrap Resampling. Contributed package. Version 1-1.10. R Foundation for Statistical Computing, Vienna. [WWW document]. URL http://www.R-project.org [accessed on 4 November 2015].
Svensson, B.G. (1979) Pyrobombus lapponicus auct., in Europe recognized as two species: P. lapponicus (Fabricius 1793) and P. monticola (Smith, 1849) (Hymenoptera, Apoidea, Bombinae). Insect Systematics & Evolution, 10, 275–296.
Taberlet, P. (1998) Biodiversity at the intraspecific level: the comparative phylogeographic approach. Journal of Biotechnology, 64, 91–100.
Thuiller, W. (2004) Patterns and uncertainties of species' range shifts under climate change. Global Change Biology, 10, 2020–2027.
Tkalcu, B. (1992) Notiz zur Nomenklatur der Alpenpopulation von Pyrobombus (Pyrobombus) monticola (SMITH, 1849) (Hym. Apoidea). Entomologische Nachrichten und Berichte, 36, 138–139.
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.
Vincenti, M., Guglielmetti, G., Cassani, G. & Tonini, C. (1987) Determination of double bond position in di unsaturated compounds by mass spectrometry of dimethyl disulfide derivatives. Analytical Chemistry, 59, 694–699.
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.
Waples, R. (1995) Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. Evolution and the Aquatic Ecosystem (ed. by J. Nielsen), pp. 8–27. American Fisheries Society, Bethesda, Maryland.
Wilcox, T.P., Zwickl, D.J., Heath, T.A. & Hillis, D.M. (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution, 25, 361–371.
Williams, P.H. (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bulletin of the Natural History Museum (Entomology), 60, 1–204.
Williams, P.H., Brown, M.J.F., Carolan, J.C. et al. (2012) Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity, 10, 21–56.
Williams, P.H., Byvaltsev, A.M., Cederberg, B. et al. (2015) Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE, 10, e0144544.
Žáček, P., Prchalová-Horňákova, D., Tykva, R. et al. (2013) De novo biosynthesis of sexual pheromone in the labial gland of bumblebee males. ChemBioChem, 14, 361–371.
Zagwijn, W.H. (1992) The beginning of the ice age in Europe and its major subdivisions. Quaternary Science Reviews, 11, 583–591.
Zink, R.M. (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society of London Series B, 271, 561–564.
Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criteria. PhD Dissertation, The University of Texas, Austin, Texas