Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs

Conservation Genetics

Volumn 9, Issue 3, 2008, Pages 653-666

  Murray, Tomás E ^a,c   Fitzpatrick, Úna ^b   Brown, Mark J F ^b   Paxton, Robert J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c TEAGASC   (Ireland)

Author keywords

Bombus; CO1; Cytochrome c oxidase subunit 1; DNA barcode; PCR RFLP

Indexed keywords

BEE; CONSERVATION MANAGEMENT; CYTOCHROME; DIVERGENCE; IDENTIFICATION METHOD; MITOCHONDRIAL DNA; MORPHOLOGY; PHYLOGENETICS; POPULATION GENETICS; SPECIES COMPLEX; SPECIES DIVERSITY; URBAN AREA;

EURASIA; EUROPE; IRELAND; WESTERN EUROPE;

BOMBUS (GENUS); BOMBUS CRYPTARUM; BOMBUS LUCORUM; BOMBUS MAGNUS; BOMBUS TERRESTRIS; INSECTA;

EID: 42549097410     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-007-9394-z     Document Type: Article

References (76)

1. Alford DV (1975) Bumblebees. Davis-Poynter, London
2. Banaszak J, Rasmont P (1994) Ocurrence and distribution of the subgenus Bombus Latreille sensu stricto in Poland (Hymenoptera, Apoidea). Pol Pismo Ent 63:337-356
3. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570-572
4. Benton T (2006) Bumblebees. Collins, London
5. Bertsch A (1997a) Abgrenzung der Hummel-Arten Bombus cryptarum und B. lucorum mittels männlicher Labialdrüsen-Sekrete und morphologischer Merkmale (Hymenoptera, Apidae). Entomol Gen 22:129-145
6. Bertsch A (1997b) Wieviele Arten der Untergattung Terrestribombus (Hymenoptera, Apidae) gibt es in Nordhessen; die Abgrenzung von Bombus cryptarum und B. lucorum mittels männlicher Labial-drüsen-Sekrete und morphologischer Merkmale. Marburger Ent Pub 2:1-28
7. Bertsch A, Schweer H, Titze A (2004) Discrimination of the bumblebee species Bombus lucorum, B. crytarum and B. magnus by morphological characters and male labial gland secretions. Beitr Ent 54:365-386
8. 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
9. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. TREE 22:148-155
10. Blaxter ML (2004) The promise of a DNA taxonomy. Philos Trans R Soc Lond B 359:669-679
11. Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linn Soc 91:161-188
12. Carvell C, Roy DB, Smart SM, Pywell RF, Preston CD, Goulson D (2006) Declines in forage availability for bumblebees at a national scale. Biol Conserv 132:481-489
13. Caterino MS, Cho S, Sperling FAH (2000) The current state of insect molecular systematics: a thriving Tower of Babel. Annu Rev Entomol 45:1-54
14. Chittka L, Ings TC, Raine NE (2004) Chance and adaptation in the evolution of island bumblebee behaviour. Popul Ecol 46:243-251
15. Cognato A (2006) Standard percent DNA sequence difference for insects does not predict species boundaries. J Econ Entomol 99:1037-1045
16. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461-467
17. Crozier RH, Crozier C (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organisation. Genetics 133:97-117
18. DeSalle R (2006) Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conserv Biol 20:1545-1547
19. DeSalle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philos Trans R Soc 360:1905-1916
20. Edwards M, Jenner M (2005) Field guide to the bumblebees of Great Britain and Ireland. Ocelli Ltd., England
21. Ellis JS, Knight ME, Goulson D (2005) Delineating species for conservation using mitochondrial sequence data: the taxonomic status of two problematic Bombus species (Hymenoptera: Apidae). J Insect Conserv 9:75-83
22. Ellis JS, Knight TM, Carvell C, Goulson D (2006) Cryptic species identification: a simple diagnostic tool for discrimination between two problematic bumblebee species. Mol Ecol Notes 6:540-542
23. Feltwell J (2006) Bumblebees. Wildlife Matters, Marlham, UK
24. Fitzpatrick Ú, Murray TE, Byrne A, Paxton RJ, Brown MJF (2006) Regional red data list of Irish bees. In: National parks and wildlife service (Ireland) and environment and heritage service (N. Ireland). Available from: http://www.npws.ie/PublicationsLiterature/RegionalRedLists/file,3658,en.pdf
25. Fitzpatrick Ú, Murray TE, Paxton RJ, Breen J, Cotton D, Santorum V, Brown MJF (2007) Rarity and decline of bumble bees - a test of causes and correlates. Biol Conserv 136:185-194
26. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press
27. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Syst 34:397-423
28. Goka K, Okabe K, Yoneda M, Niwa S (2001) Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol Ecol 10:2095-2099
29. Goulson D (2003) Bumblebees: their behaviour and ecology. Oxford University Press, Oxford
30. Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME (2005) Causes of rarity in bumblebees. Biol Conserv 122:1-8
31. Goulson D, Hanley ME, Darvill B, Ellis JS (2006) Biotope associations and the decline of bumblebees (Bombus spp.). J Insect Conserv 10:95-103
32. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond Ser B 270:313-321
33. Hebert PDN, Ratnasingham S, deWaard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond Ser B 270:S96-S99
34. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812-14817
35. Holehouse KA, Hammond RL, Bourke AFG (2003) Non-lethal sampling of DNA from bumble bees for conservation genetics. Insectes Soc 50:277-285
36. Ings TC, Schikora J, Chittka L (2005) Bumblebees, humble pollinators or assiduous invaders? A population comparison of foraging performance in Bombus terrestris. Oceologia 144:508-516
37. Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940-948
38. IBRA (1980) Atlas of the bumblebees of the British Isles. Institute of Terrestrial Ecology and International Bee Research Association, Cambridge, UK
39. IUCN (2001) IUCN red list categories and criteria, version 3.1. IUCN Species Survival Commission, Gland, Switzerland
40. IUCN (World Conservation Union) (2003) Guidelines for application of IUCN red list criteria at regional levels: version 3.0. IUCN Species Survival Commission. IUCN, Gland, Switzerland
41. IUCN (World Conservation Union) (2006) Guidelines for using the IUCN red list categories and criteria, version 6.1. IUCN Species Survival Commission. IUCN, Gland, Switzerland. Available from http://www.intranet.iucn.org/webfiles/ doc/SSC/RedList/RedListGuidelines.pdf
42. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83-112
43. Kosior A, Celary W, Olejniczak P, Fijal J, Król W, Solarz W, Plonka P (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:79-88
44. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163
45. Løken A (1973) Studies on Scandinavian bumble bees (Hymenoptera, Apidae). Norsk Entomol Tidsskrift 20:1-218
46. Mallet J (1995) A species definition for the modern synthesis. TREE 10:294-299
47. Mallet J (2007) Species, concepts of. In: Levin SA et al (eds) Encyclopedia of biodiversity, vol 5, 2nd edn. Academic Press, San Diego, CA, pp 427-440
48. Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:2229-2238
49. Mitsuhata M, Ono M (1996) Hybridization between Japanese and European bumblebees (Bombus spp.). In: Summaries of the 7th international pollination symposium. Lethbridge, Canada
50. Monaghan MT, Balke M, Gregory TR, Vogler AP (2005) DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philos Trans R Soc Lond B 360:1925-1933
51. Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357-358
52. Pamilo P, Tengö J, Rasmont P, Pirhonen K, Pekkarinen A, Kaarnama E (1997) Pheromonal and enzyme genetic characteristics of the Bombus lucorum species complex in northern Europe. Entomol Fenn 14:187-194
53. Paxton RJ, Thorén PA, Tengo J, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511-519
54. Pedersen BV (2003) European bumblebees (Hymenoptera: Bombini) - phylogenetic relationships inferred from DNA sequences. Insect Syst Evol 33:361-386
55. Prŷs-Jones OE, Corbet SA (1991) Bumblebees. Naturalists' handbook series 6. Richmond Publishing Co., Slough, UK
56. Rasmont P (1984) Les bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale. Spixiana 7:136-160
57. Rasmont P, Scholl A, de Jonghe R, Obrecht E, Adamski A (1986) Identité et variabilité des mâles de bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae, Bombinae). Rev Suisse Zool 93:661-682
58. Riddle BR, Hafner DJ, Alexander LF (2000) Phylogeny and systematics of Peromyscus eremicus species group and the historical biogeography of North American warm regional deserts. Mol Phylogenet Evol 17:145-160
59. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574
60. Rubinoff D (2006) Utility if mitochondrial DNA barcodes in species conservation. Conserv Biol 20:1026-1033
61. Savolainen V, Cowan RS, Vogler AP, Roderick GK, Lane R (2005) Towards writing the encyclopedia of life: an introduction to DNA barcoding. Philos Trans R Soc B 360:1805-1811
62. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann Entomol Soc Am 87:651-701
63. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzes. Mol Biol Evol 10:512-526
64. Tanaka H, Roubik DW, Kato M, Liew F, Gunsalam G (2001) Phylogenetic position of Apis nuluensis of northern Borneo and phylogeography of A. cerana as inferred from mitochondrial DNA sequences. Insectes Soc 48:44-51
65. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
66. Velthuis HHW, 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
67. von Hagen E (2003) Hummeln: bestimmen, ansiedeln, vermehren, schützen. Fauna-Verlag, Nottuln
68. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506-513
69. Wells MM, Henry CS (1998) Songs, reproductive isolation, and speciation in cryptic species of insect: a case study using green lacewings. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 217-233
70. Westrich P (1989) Die Wildbienen Baden Württembergs, vol 2. Verlag Eugen Ulmer, Stuttgart
71. Williams PH (1986) Environmental change and the distributions of British bumble bees (Bombus Latr.). Bee World 67:50-61
72. Williams PH (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bull Nat Hist Mus Lond (Entomol) 60:1-204
73. Williams PH (1998) An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bull Nat Hist Mus Lond (Entomol) 67:79-152
74. Williams PH (2000) Are Bombus lucorum and magnus separate species? BWARS Newslett 1:15-17
75. Williams PH (2005) Does specialization explain rarity and decline among British bumblebees? a response to Goulson et al. Biol Conserv 122:33-43
76. Williams PH, Hernandez LM (2000) Distinguishing females of the bumble bees Bombus ruderatus (F.) from Bombus hortorum (L.) in Britain: a preliminary application of quantitative techniques. In: Report to the UK biodiversity action plan bumblebee working group. The Natural History Museum, London