Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae)

Molecular Ecology

Volumn 15, Issue 14, 2006, Pages 4375-4386

  Ellis, J S ^a   Knight, M E ^b   Darvill, B ^a   Goulson, D ^c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Bombus; Conservation; Microsatellites; Nest density; Population genetics

Indexed keywords

ANIMAL; ARTICLE; BEE; CLASSIFICATION; DIPLOIDY; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; MALE; POPULATION DENSITY; UNITED KINGDOM;

ANIMALS; BEES; DIPLOIDY; GEOGRAPHY; GREAT BRITAIN; MALE; POPULATION DENSITY; VARIATION (GENETICS);

APIDAE; BOMBUS SYLVARUM; HYMENOPTERA; INSECTA;

EID: 33750973407     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2006.03121.x     Document Type: Article

References (76)

1. Abramson JH, Gahlinger PM (2001) Computer programs for epidemiologists: PEPI version 4.0. Sagebrush Press, Salt Lake City, Utah.
2. Anderson EC (2005) An efficient Monte Carlo method for estimating Ne from temporally spaced samples using a coalescent-based likelihood. Genetics, 170, 955-967.
3. Batra WT (1995) Bees and pollination in our changing environment. Apidologie, 26, 361-370.
4. Beekman M, van Stratum P, Veerman A (1999) Selection for nondiapause in the bumblebee Bombus terrestris, with notes on the effect of inbreeding. Entomologia Experimentalis et Applicata, 93, 6975.
5. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. Journal of Heredity, 93, 153-154.
6. Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science, 263, 485-486.
7. Carvalho GA (2001) The number of sex alleles (CSD) in a bee population and its practical importance (Hymenoptera: Apidae). Journal of Hymenoptera Research, 10, 10-15.
8. Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecology Letters, 4, 650-662.
9. Cole BJ, Wiernasz DC (1997) Inbreeding in a lek-mating ant species Pogonomyrmex occidentalis. Behavioural Ecology and Sociobiology, 40, 79-86.
10. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends in Ecology & Evolution, 10, 281-286.
11. Corbet SA, Williams IH, Osborne JL (1991) Bees and the pollination of crops and wild flowers in the European Community. Bee World, 72, 47-59.
12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014.
13. Darvill B, Knight ME, Goulson D (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos, 107, 471-478.
14. Darvill B, Ellis JS, Lye GC, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum, (Hymenoptera: Apidae). Molecular Ecology, 15, 601-611.
15. Dieringer D, Schlötterer C (2002) Microsatellite analyser (msa): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3, 167-169.
16. Duchateau MJ, Hoshiba H, Velthius HHW (1994) Diploid males in the bumblebee Bombus terrestris. Entomologica Experimentalis et Applicata, 71, 263-269.
17. Edwards M (1999) U.K.B.A.P. Bumblebee working group report. Privately distributed, Midhurst, Sussex.
18. Edwards M (2000) U.K.B.A.P. Bumblebee working group report. Privately distributed, Midhurst, Sussex.
19. Edwards M (2001) U.K.B.A.P. Bumblebee working group report. Privately distributed, Midhurst, Sussex.
20. Edwards M (2002) U.K.B.A.P. Bumblebee working group report. Privately distributed, Midhurst, Sussex.
21. Edwards M (2003) U.K.B.A.P. Bumblebee working group report. Privately distributed, Midhurst, Sussex.
22. Edwards R, Telfer MG, eds. (2001) Provisional atlas of the aculeate Hymenoptera of Britain and Ireland. Part 3. Biological Records Centre, Huntingdon, UK.
23. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics, 92, 832-839.
24. Estoup A, Scholl A, Pouvreau A, Solignac M (1995a) Monoandry and polyandry in bumblebees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Molecular Ecology, 4, 89-93.
25. Estoup A, Tailliez C, Cornuet J-M, Solignac M (1995b) Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Molecular Biology and Evolution, 12, 1074-1084.
26. Estoup A, Solignac M, Cornuet J-M, Goudet J, Scholl A (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology, 5, 19-31.
27. Frankham R (2005) Genetics and extinction. Biological Conservation, 126, 131-140.
28. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press, New York.
29. Fussell M, Corbet SA (1992) Forage for bumblebees and honey bees in farmland: a case study. Journal of Apicultural Research, 30, 87-97.
30. Fussell M, Corbet SA (1993) Bumblebee (Hym., Apidae) forage plants in the United Kingdom. Entomologist's Monthly Magazine, 129, 1-15.
31. Gerloff CU, Schmid-Hempel P (2005) Inbreeding depression and family variation in a social insect, Bombus terrestris, (Hymenoptera: Apidae). Oikos, 111, 67-80.
32. Gerloff CU, Ottmer BK, Schmid-Hempel P (2003) Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology, 17, 582-589.
33. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Molecular Ecology, 8, 1231-1234.
34. Goudet J (2001) FSTAT: A Program To Estimate and Test Gene Diversities and Fixation Indices (version 2.9.3). Available from http://www.unil.ch/izea/ softwares/fstat.html.
35. Goulson D (2003) Bumblebees: Their Behaviour and Ecology. Oxford University Press, Oxford.
36. Gyllenstrand N, Seppa P (2003) Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape. Molecular Ecology, 12, 2931-2940.
37. Hasegawa E, Yamaguchi T (1995) Population structure, local mate competition and sex-allocation pattern in the ant Messor aciculatus. Evolution, 49, 260-265.
38. Henter HJ (2003) Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa. Evolution, 57, 1793-1803.
39. Holehouse KA, Hammond RL, Bourke AFG (2003) Non-lethal sampling of DNA from bumblebees for conservation genetics. Insectes Sociaux, 50, 277-285.
40. Holloway AK, Heimpel GE, Strand MR, Antolin MF (1999) Survival of diploid males in Bracon sp. near hebetor (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 92, 110-116.
41. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 53, 1898-1914.
42. Johansson M, Primmer CR, Merila J (2006) History vs. current demography: explaining the genetic population structure of the common frog (Rana temporaria). Molecular Ecology, 15 (4), 975-983.
43. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends in Ecology &Evolution, 17, 230-241.
44. Knight ME, Bishop S, Martin AP et al. (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Molecular Ecology, 14, 1811-1820.
45. Koisor A (1995) Changes in the fauna of bumble-bees (Bombus Latr.) and cuckoo-bees (Psithyrus Lep.) of selected regions in southern Poland. In: Changes in Fauna of Wild bees in Europe (ed. Banaszak J), pp. 103-111. Pedagogical University, Bydgoszcz, Poland.
46. Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology, 12, 228-237.
47. Muller CB, Schmid-Hempel P (1992) Correlates of reproductive success among field colonies of B. lucorum: the importance of growth and paraites. Ecological Entomology, 17, 343-353.
48. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
49. Packer L, Owen R (2001) Population genetic aspects of pollinator decline. Conservation Ecology, 5, art. No 4 June 2001.
50. Paxton RJ, Thoren PA, Gyllenstrand N, Tengo J (2000) Microsatellite DNA analysis reveals low diploid male production in a communal bee with inbreeding. Biological Journal of the Linnean Society, 69, 483-502.
51. Peterson MA, Denno RF (1998) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. American Naturalist, 152, 428-446.
52. Pirounakis K, Koulianos S, Schmid-Hempel P (1998) Genetic variation among European populations of Bombus pascuorum (Hymenoptera: Apidae) from mitochondrial DNA sequence data. European Journal of Entomology, 95, 27-33.
53. Plowright RC, Pallett MJ (1979) Worker-male conflict and inbreeding in bumblebees (Hymenoptera: Apidae). Canadian Entomologist, 111, 289-294.
54. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution, 11, 201-206.
55. Rasmont P (1995) How to restore the Apoid diversity in Belgium and France? Wrong and right ways, or the end of the protection paradigm! In: Changes in Fauna of Wild Bees in Europe (ed. Banaszak J), pp. 53-63. Pedagogical University, Bydgoszcz, Poland.
56. Raymond M, Rousset F (1995) GENEPOP 1.2: a population genetics software for exact tests and ecumenism. Journal of Heredity, 86, 248-249. Available from http://wbiomed.curtin.edu.au/genepop.
57. Rice WR (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
58. Ross KG, Fletcher DJC (1986) Diploid male production- a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera, Formicidae). Behavioural Ecology and Sociobiology, 19, 283-291.
59. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228.
60. Saccheri I, Kuusaari M, Kankare M et al. (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
61. Schmitt T, Hewitt GM (2004) The genetic pattern of population threat and loss: a case study of butterflies. Molecular Ecology, 13, 21-31.
62. Shao ZY, Mao HX, Fu WJ et al. (2004) Genetic structure of Asian populations of Bombus ignitus (Hymenoptera: Apidae). Journal of Heredity, 95, 46-52.
63. Sorati M, Neuna M, Hoffmann AA (1996) Inbreeding and incompatability in Trichogramma, brassicae: evidence and implications for quality control. Entomologia Experimentalis et Applicata, 78, 283-290.
64. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences, USA, 101, 15261-15264.
65. Sundstrom C, Keller L, Chapuisat M (2003) Inbreeding and sex-biased gene flow in the ant Formica exsecta. Evolution, 57, 1552-15561.
66. Truett GE, Heeger P, Mynatt RL et al. (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques, 29, 52-+;.
67. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population-structure. Evolution, 38, 1358-1370.
68. Widmer A, Schmid-Hempel P (1999) The population genetic structure of a large temperate pollinator species Bombus pascuorum (Scopoli) (Hymenoptera: Apidae). Molecular Ecology, 8, 387-398.
69. Widmer A, Schmid-Hempel P, Estoup A, Scholl A (1998) Population genetic structure and colonization history of Bombus terrestris s.1. (Hymenoptera: Apidae) from the Canary Islands and Madeira. Heredity, 81, 563-572.
70. Williams PH (1982) The distribution and decline of British bumblebees (Bombus Latr.). Journal of Apicultural Research, 21, 236-245.
71. Williams PH (1986) Environmental change and the distributions of British bumblebees (Bombus Latr.). Bee World, 67, 50-61.
72. Wright S (1933) Inbreeding and homozygosis. Proceedings of the National Academy of Sciences, USA, 19, 411-420.
73. Wright S (1951) The genetical structure of populations. Annals of Eugenics, 15, 323-354.
74. Zayed A, Packer L (2001) High levels of diploid male production in a primitively eusocial bee (Hymenoptera: Halictidae). Heredity, 87, 631-636.
75. Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences, USA, 102, 10742-10746.
76. Zayed A, Roubik DW, Packer L (2004) Use of diploid male frequency data as an indicator of pollinator decline. Proceedings of the Royal Society of London. Series B, Biological Sciences, 271, S9-S12.