[en] Many islands are biodiversity hotspots that host numerous endemic species. Unfortunately, insular faunas suffer from high rates of extinction and endangerment, and numerous conservation plans have been developed for their protection. These conservation plans are often assessed on the basis of occurrence and proportion of endemic taxa. However, delimitations of species and subspecies are still confusing and controversial. From a practical point of view, these disagreements make it difficult for government agencies and non-governmental organizations to initiate conservation measures. The present study develops a pragmatic integrative taxonomic approach on the basis of molecular and eco-chemical criteria. This
method is applied to the insular bumblebee fauna of Corsica. For each taxon, the differentiation of Corsican taxa from the nearest related allopatric parents is characterized using genetic markers and the chemical composition of cephalic labial gland secretions. Phylogenetic analyses, Bayesian implementation of the
general mixed Yule-coalescent approach, and comparative chemical studies show that two Corsican taxa can be considered as endemic species while five others can be considered as subspecies. Regardless of the taxonomic assessment the method facilitates diagnosis of evolutionarily significant units and rank taxa according to their distinctiveness. International Union for Conservation of Nature red lists are
reconsidered according to the new taxonomic hypothesis for Corsican bumblebees. Modifications in species assessments are proposed. The present approach provides useful data sets for policy-makers and conservation organizations.
Agapow, P.-M., Bininda-Emonds, O.R.P., Crandall, K.A., Gittleman, J.L., Mace, G.M., Marshall, J.C. & Purvis, A. (2004). The impact of species concept on biodiversity studies. Q. Rev. Biol. 79, 161-179.
Appelgren, M., Bergström, G., Svensson, B.G. & Cederberg, B. (1991). Marking pheromones of Megabombus bumble bee males. Acta Chem. Scand. 45, 972-974.
Avise, J.C. (2000). Phylogeography: the history and formation of species: Cambridge: Harvard University Press.
Avise, J.C. (2004). What is the field of biogeography, and where is it going? Taxon 53, 893-898.
Ayasse, M., Paxton, R.J. & Tengö, J. (2001). Mating behavior and chemical communication in the order Hymenoptera. Annu. Rev. Entomol. 59, 299-319.
Baer, B. (2003). Bumblebees as model organisms to study male sexual selection in social insects. Behav. Ecol. Sociobiol. 54, 521-533.
Barraclough, T.G., Birky, C.W. Jr. & Burt, A. (2003). Diversification in sexual and asexual organisms. Evolution (N. Y.) 57, 2166-2172.
Barraclough, T.G., Hughes, M., Ashford-Hodges, N. & Fujisawa, T. (2009). Inferring evolutionarily significant units of bacterial diversity from broad environmental surveys of single-locus data. Biol. Lett. 5, 425-428.
Bauer, A.M., Parham, J.F., Brown, R.M., Stuart, B.L., Grismer, L., Papenfuss, T.J., Böhme, W., Savage, J.M., Carranza, S., Grismer, J.L., Wagner, P., Schmitz, A., Ananjeva, N.B. & Inger, R.F. (2011). Availability of new Bayesian-delimited gecko names and the importance of character-based species descriptions. Proc. Roy. Soc. Lond. Ser. B. 278, 490-493.
Bertsch, A. & Schweer, H. (2012). 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? Beitr. Ent. 62, 103-124.
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 Soc. 52, 45-54.
Boursot, P. & Bonhomme, F. (1986). Génétique et évolution du génome mitochondrial des Métazoaires. Genet. Sel. Evol. 18, 73-78.
Brower, A.V.Z. (1994). Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA 91, 6491-6495.
Calam, D.H. (1969). Species and sex-specific compounds from the heads of male bumblebees (Bombus spp. Nature 221, 856-857.
Cameron, S.A., Hines, H.M. & Williams, P.H. (2007). A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linn. Soc. 91, 161-188.
Carolan, J.C., Murray, T.E., Fitzpatrick, U., Crossley, J., Schmidt, H., Cederberg, B., McNally, L., Paxton, R.J., Williams, P.H. & Brown, M.J.F. (2012). Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS ONE 7, e29251.
Cederberg, B., Michez, D., Nieto, A., Radchenko, V., Rasmont, P. & Roberts, S. (2013). Bombus In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Downloaded on 01 Januray 2014. http://www.iucnredlist.org (accessed 2 January 2014).
Collar, N. (1994). Extinction, endangerment and everything. World Birdwatch 16, 6-9.
Conner, J. (2004). A primer of ecological genetics. Sunderland: Sinauer Associates.
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). Conserv. Genet. 12, 637-646.
Cruaud, A., Gautier, M., Galan, M., Foucaud, J., Sauné, L., Genson, G., Dubois, E., Nidelet, S., Deuve, T. & Rasplus, J.-Y. (2014). Empirical assessment of RAD sequencing for interspecific phylogeny. Mol. Biol. Evol. 31, 1272-1274.
De Jonghe, R. (1986). Crossing experiments with Bombus terrestris terrestris (Linnaeus, 1758) and Bombus terrestris xanthopus Kricehbaumer, 1870 and some notes on diapause and nosemose (Hymenoptera: Apoidea). Phegea 14, 19-23.
De Meulemeester, T., Gerbaux, P., Boulvin, M., Coppée, A. & Rasmont, P. (2011). A simplified protocol for bumblebee species identification by cephalic secretion analysis. Insectes Soc. 58, 227-236.
De Queiroz, K. (2007). Species concepts and species delimitation. Syst. Biol. 56, 879-886.
Dellicour, S. & Lecocq, T. (2013). GCALIGNER 1.0: an alignment program to compute a multiple sample comparison data matrix from large eco-chemical datasets obtained by gas chromatography. J. Sep. Sci. 36, 3206-3209.
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
Dufrêne, M. & Legendre, P. (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345-366.
Esselstyn, J.A., Evans, B.J., Sedlock, J.L., Khan, F.A.A. & Heaney, L.R. (2012). Single-locus species delimitation: a test of the mixed Yule-coalescent model, with an empirical application to Philippine round-leaf bats. Proc. Roy. Soc. Lond. Ser. B. 279, 3678-3686.
Ferguson, J.W.H. (2002). On the use of genetic divergence for identifying species. Biol. J. Linn. Soc. 75, 509-516.
Fisher, B.L. & Smith, M.A. (2008). A revision of Malagasy species of Anochetus Mayr and Odontomachus Latreille (Hymenoptera: Formicidae). PLoS ONE 3, e1787.
Fisher, R. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.
Frankham, R., Ballou, J.D. & Briscoe, D.A. (2010). Introduction to conservation genetics. 2nd edn. Cambridge: Cambridge University Press.
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. Syst. Biol. 62, 707-724.
Haig, S.M., Beever, E.A., Chambers, S.M., Draheim, H.M., Dugger, B.D., Dunham, S., Elliott-Smith, E., Fontaine, J.B., Kesler, D.C., Knaus, B.J., Lopes, I.F., Loschl, P., Mullins, T.D. & Sheffield, L.M. (2006). Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conserv. Biol. 20, 1584-1594.
Hasselrot, T.B. (1960). Studies on Swedish bumblebees (genus Bombus Latr.), their domestication and biology. Opusc. Entomol. (Suppl.) 17, 1-192.
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.
Hillis, D.M. & Bull, J.J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42, 182-192.
Isaac, N.J.B., Mallet, J. & Mace, G.M. (2004). Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol. Evol. 19, 464-469.
IUCN Species Survival Commission (2012). Guidelines for application of IUCN red list criteria at regional and national levels version 4.0. Gland: IUCN.
Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066.
Kier, G., Kreft, H., Tien, M.L., Jetz, W., Ibisch, P.L., Nowicki, C., Mutke, J. & Barthlott, W. (2009). A global assessment of endemism and species richness across island and mainland regions. Proc. Natl. Acad. Sci. USA 106, 9322-9327.
Kruckenhauser, L., Duda, M., Bartel, D., Sattmann, H., Harl, J., Kirchner, S. & Haring, E. (2014). Paraphyly and budding speciation in the hairy snail (Pulmonata, Hygromiidae). Zool. Scr. 43, 273-288.
Kuhlmann, M., Else, G.R., Dawson, A. & Quicke, D.L.J. (2007). Molecular, biogeographical and phenological evidence for the existence of three western European sibling species in the Colletes succinctus group (Hymenoptera: Apidae). Org. Divers. Evol. 7, 155-165.
Kullenberg, B., Bergström, G., Bringer, B., Carlberg, B. & Cederberg, B. (1973). Observations on scent marking by Bombus Latr. and Psithyrus Lep. males (Hym., Apidae) and localization of site of production of the secretion. Zoon (Suppl.) 1, 23-30.
Lecocq, T., Lhomme, P., Michez, D., Dellicour, S., Valterová, I. & Rasmont, P. (2011). Molecular and chemical characters to evaluate species status of two cuckoo bumblebees: Bombus barbutellus and Bombus maxillosus (Hymenoptera, Apidae, Bombini). Syst. Entomol. 36, 453-469.
Lecocq, T., Dellicour, S., Michez, D., Lhomme, P., Vanderplanck, M., Valterová, I., Rasplus, J.-Y. & Rasmont, P. (2013a). Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BMC Evol. Biol. 13, 263.
Lecocq, T., Vereecken, N.J., Michez, D., Dellicour, S., Lhomme, P., Valterová, I., Rasplus, J.-Y. & Rasmont, P. (2013b). Patterns of genetic and reproductive traits differentiation in mainland vs. Corsican populations of bumblebees. PLoS ONE 8, e65642.
Leys, R., Cooper, S.J.B. & Schwarz, M.P. (2002). Molecular phylogeny and historical biogeography of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae). Biol. J. Linn. Soc. 77, 249-266.
Lhomme, P., Ayasse, M., Valterová, I., Lecocq, T. & Rasmont, P. (2012). Born in an alien nest: how do social parasite male offspring escape from host aggression? PLoS ONE 7, e43053.
Lhomme, P., Sramkova, A., Kreuter, K., Lecocq, T., Rasmont, P. & Ayasse, M. (2013). A method for year-round rearing of cuckoo bumblebees (Hymenoptera: Apoidea: Bombus subgenus Psithyrus). Ann. Soc. Entomol. Fr. 49, 37-41.
Maddison, W.P. (1997). Gene trees in species trees. Syst. Biol. 46, 523-536.
Martens, J. (1996). Vocalizations and speciation of Palearctic birds. In Ecology and evolution of acoustic communication in birds: 221-240. Kroodsma, D.E. & Miller, E.H. (Eds). Ithaca: Comstock Publishing.
Mayden, R. (1997). A hierarchy of species concepts: the denouement in the saga of the species problem. In Species: the units of biodiversity: 381-424. Claridge, M.F., Dawah, H.A. & Wilson, M.R. (Eds). London: Chapman and Hall Ltd.
Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.
Oksanen, F.J., Blanchet, G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H. & Wagner, H. (2011). Vegan: community ecology package. Tertiary Vegan: Community Ecology Package.
Paterson, H.E.H. (1993). Evolution and the recognition concept of species. Baltimore: The Johns Hopkins University Press.
Pedersen, B.V. (2002). European bumblebees (Hymenoptera: Bombini) - phylogenetic relationships inferred from DNA sequences. Insect Syst. Evol. 33, 361-386.
Peterson, A.T. & Navarro-Sigüenza, A.G. (1999). Alternate species concepts as bases for determining priority conservation areas. Conserv. Biol. 13, 427-431.
Phillimore, A.B. & Owens, I.P.F. (2006). Are subspecies useful in evolutionary and conservation biology? Proc. R. Soc. B Biol. Sci. 273, 1049-1053.
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. Syst. Biol. 55, 595-609.
Posada, D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253-1256.
R Development Core Team (2013). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org (accessed 2 January 2014).
Rasmont, P. & Adamski, A. (1996). Les Bourdons de la Corse (Hymenoptera, Apoidea, Bombinae). Notes fauniques de Gembloux 31, 1-87.
Rasmont, P. & Iserbyt, S. (2012). Atlas of the European bees: genus Bombus. STEP Project. Status Trends Eur. Pollinators, Tertiary Atlas of the European Bees: genus Bombus. STEP Project. http://www.zoologie.umh.ac.be//hymenoptera/page.asp?ID=169 (accessed 2 January 2014).
Rasmont, P., Coppée, A., Michez, D. & De Meulemeester, T. (2008). An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Ann. Soc. Entomol. Fr. 44, 243-250.
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 Evol. Biol. 12, 196.
Ronquist, F. & Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
Rosenthal, G.G. & Stuart-Fox, D. (2012). Environmental disturbance and animal communication. In Behavioural responses to a changing world: 17-31. Candolin, U. & Wong, B.B.M. (Eds). Oxford: Oxford University Press.
Salvato, P., Battisti, A., Concato, S., Masutti, L., Patarnello, T. & Zane, L. (2002). Genetic differentiation in the winter pine processionary moth (Thaumetopoea pityocampa - wilkinsoni complex), inferred by AFLP and mitochondrial DNA markers. Mol. Ecol. 11, 2435-2444.
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. Annu. Rev. Entomol. 55, 421-438.
Symonds, M.R.E., Moussalli, A. & Elgar, M.A. (2009). The evolution of sex pheromones in an ecologically diverse genus of flies. Biol. J. Linn. Soc. 97, 594-603.
Tang, C.Q., Leasi, F., Obertegger, U., Kieneke, A., Barraclough, T.G. & Fontaneto, D. (2012). The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc. Natl. Acad. Sci. USA 109, 16208-16212.
Trewick, S.A. (2008). DNA barcoding is not enough: mismatch of taxonomy and genealogy in New Zealand grasshoppers (Orthoptera: Acrididae). Cladistics 24, 240-254.
Urbanová, K., Halák, J., Hovorka, O., Kindl, J. & Valterová, I. (2004). Marking pheromones of the cuckoo bumblebee males (Hymenoptera, Apoidea, Bombus Latreille): compositions of labial gland secretions of six species found in the Czech Republic. Biochem. Syst. Ecol. 32, 1025-1045.
Velthuis, H.H.W. & van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37, 421-451.
Venables, W.N. & Ripley, B.D. (2002). Modern applied statistics with S. 4th edn. New York: Springer.
Vereecken, N.J., Mant, J. & Schiestl, F.P. (2007). Population differentiation in female sex pheromone and male preferences in a solitary bee. Behav. Ecol. Sociobiol. 61, 811-821.
Whittaker, R.J. & Fernández-Palacios, J.M. (2007). Island biogeography - ecology, evolution, and conservation. 2nd edn. Oxford: Oxford University Press.
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. Mol. Phylogenet. Evol. 25, 361-371.
Williams, P.H., An, J., Brown, M.J.F., Carolan, J.C., Goulson, D., Huang, J. & Ito, M. (2012a). Cryptic bumblebee species: consequences for conservation and the trade in greenhouse pollinators. PLoS ONE 7, e32992.
Williams, P.H., Brown, M.J.F., Carolan, J.C., An, J., Goulson, D., Aytekin, A.M., Best, L.R., Byvaltsev, A.M., Cederberg, B., Dawson, R., Huang, J., Ito, M., Monfared, A., Raina, R.H., Schmid-Hempel, P., Sheffield, C.S., Šima, P. & Xie, Z. (2012b). Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae). Syst. Biodivers. 10, 21-56.
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869-2876.
Zwickl, D.J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criteria. D. Phil. Thesis, The University of Texas at AustinEditor, Austin, Texas.
Žáček, P., Prchalová-Hornákov, D., Tykva, R., Kindl, J., Vogel, H., Svatoš, A., Pichová, I. & Valterová, I. (2013). De novo biosynthesis of sexual pheromone in the labial gland of bumblebee males. Chembiochem 14, 361-371.
