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Genetic origins of honey bees (Apis mellifera) on Kangaroo Island and Norfolk Island (Australia) and the Kingdom of Tonga

  • Nadine C. Chapman
  • Jiani Sheng
  • Julianne Lim
  • Samuel F. Malfroy
  • Brock A. Harpur
  • Amro Zayed
  • Michael H. Allsopp
  • Thomas E. Rinderer
  • John M. K. Roberts
  • Emily J. Remnant
  • Benjamin P. Oldroyd
Original article


We examine the origin of honey bee (Apis mellifera) populations in Kangaroo Island (Australia), Norfolk Island (Australia) and the Kingdom of Tonga using a highly polymorphic mitochondrial DNA region and a panel of 37 single nucleotide polymorphisms that assigns ancestry to three evolutionary lineages: Eastern Europe, Western Europe and Africa. We also examine inbreeding coefficients and genetic variation using microsatellites and mitochondrial sequencing. The honey bees of Kangaroo Island have a high proportion of Eastern European ancestry (90.2%), consistent with claims that they are of the subspecies A. m. ligustica. The honey bees of Norfolk Island also had a majority of ancestry from Eastern Europe (73.1%) with some contribution from Western Europe (21.2%). The honey bees of Tonga are mainly of Western European (70.3%) origin with some Eastern European ancestry (27.4%). Despite the suspected severe bottlenecks experienced by these island population, inbreeding coefficients were low.


Apis mellifera ancestry assignment population genetics isolated populations single nucleotide polymorphisms 



We thank Peter Davis for collecting bees from Kangaroo Island, Bruce White and Lamorna Osborne for collecting bees from Tonga and the beekeepers of Norfolk Island for providing access to their colonies to SFM. We thank two anonymous reviewers for their helpful comments which improved the manuscript.

Author contributions

NCC, BPO, SFM, JMKR and EJR designed the experiment. NCC and JS extracted DNA and performed genotyping. NCC performed data analysis. AZ and BAH provided SNPs and data. NCC, BPO, SFM, JMKR, EJR, JL, MHA and TER provided samples. NCC and BPO wrote the paper, with suggestions from co-authors. All authors read and approved the article prior to publication.

Funding information

This project was supported by Rural Industries Research and Development Corporation (AgriFutures) Australia PRJ-007774 (BPO), Science and Innovation Award for Young People in Agriculture, Fisheries and Forestry: CSIRO Biosecurity Flagship 2015 (NCC), Natural Sciences and Engineering Research Council Canada Discovery grant (AZ), Ontario Ministry of Research and Innovation’s Early Researcher Award (AZ), Natural Sciences and Engineering Research Council Canada Postdoctoral Fellowship (BAH), Australian and Pacific Science Foundation grant APSF15-02 (EJR), the Australian Government and the Norfolk Island Administration (SFM) and Rural Industries Research and Development Corporation (AgrFutures) Australia PRJ-008540 (JMKR).

Supplementary material

13592_2018_615_MOESM1_ESM.docx (19 kb)
ESM 1. (DOCX 18 kb)


  1. Adam B. (1983) In Search of the Best Strains of Bees. Northern Bee Books, Hebden Bridge, West Yorkshire, United Kingdom.Google Scholar
  2. Alburaki M., B. Bertrand, H. Legout, S. Moulin, A. Alburaki, et al. (2013) A fifth major genetic group among honeybees revealed in Syria. BMC Genetics 14: 117.CrossRefGoogle Scholar
  3. Anderson D.L. (1990) Pests and pathogens of the honeybee (Apis mellifera L.) in Fiji. Journal of Apicultural Research 29: 53–59.CrossRefGoogle Scholar
  4. Arundel J., B.P. Oldroyd, S. Winter. (2012) Modelling honey bee queen mating as a measure of feral colony density. Ecological Modelling 247: 48–57.CrossRefGoogle Scholar
  5. Badino G., G. Celebrano, A. Manino. (1982) Genetic variability of Apis mellifera ligustica Spin. in a marginal area of its geographic distribution. Experientica 38: 540–541.CrossRefGoogle Scholar
  6. Badino G., G. Celebrano, A. Manino. (1983) Population structure and Mdh-1 locus variation in Apis mellifera ligustica. Journal of Heredity 74: 443–446.CrossRefGoogle Scholar
  7. Barrett P. (1996) The Immigrant Bees 1788 to 1898: A Cyclopaedia on the Introduction of European Honeybees into Australia and New Zealand. P Barrett, Springwood, NSW, Australia.Google Scholar
  8. Barrett P. (2010a) A history of the introduction of honey bees into Fiji. P. Barrett, Caloundra, Queensland, Australia.Google Scholar
  9. Barrett P. (2010b) Kangaroo Island: the isle of (almost) forgotten bees. P. Barrett, Springwood, NSW, Australia.Google Scholar
  10. Beye M., M. Hasselmann, M.K. Fondrk, R.E. Page, S.W. Omholt. (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114: 419–429.CrossRefGoogle Scholar
  11. Chapman N.C., A.L. Bourgeois, L.D. Beaman, J. Lim, B.A. Harpur, et al. (2017) An abbreviated SNP panel for ancestry assignment of honeybees (Apis mellifera). Apidologie 48: 776–783.CrossRefGoogle Scholar
  12. Chapman N.C., B.A. Harpur, J. Lim, T.E. Rinderer, M.H. Allsopp, et al. (2015) A SNP test to identify Africanized honeybees via proportion of ‘African’ ancestry. Molecular Ecology Resources 15: 1346–1355.CrossRefGoogle Scholar
  13. Chapman N.C., B.A. Harpur, J. Lim, T.E. Rinderer, M.H. Allsopp, et al. (2016) Hybrid origins of Australian honeybees (Apis mellifera). Apidologie 47: 26–34.CrossRefGoogle Scholar
  14. Chapman N.C., J. Lim, B.P. Oldroyd. (2008) Population genetics of commerical and feral honey bees in Western Australia. Journal of Economic Entomology 101: 272–277.CrossRefGoogle Scholar
  15. Chávez-Galarza J., L. Garnery, D. Henriques, C.J. Neves, W. Loucif-Ayad, et al. (2017) Mitochondrial DNA variation of Apis mellifera iberiensis: further insights from a large-scale study using sequence data of the tRNAleu-cox2 intergenic region. Apidologie 48: 533–544.CrossRefGoogle Scholar
  16. Cook V.A. (1967) Facts about beekeeping in New Zealand. Bee World 48: 88–100.CrossRefGoogle Scholar
  17. Cornuet J.M. (1986) Population Genetics, in: Rinderer T.E. (Ed.), Bee Genetics and Breeding, Academic Press, Orlando, Florida, USA, pp. 235–254.Google Scholar
  18. Crane E. (1983) The Archaeology of Beekeeping. Cornell University Press, Ithaca, NY, USA.Google Scholar
  19. Crozier R.H., Y.C. Crozier. (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133: 97–117.PubMedPubMedCentralGoogle Scholar
  20. Ding G., H. Xu, B.P. Oldroyd, R. Gloag. (2017) Extreme polyandry aids the establishment of invasive populations of a social insect. Heredity 119: 318–387.CrossRefGoogle Scholar
  21. Donovan B.J. (1980) Interactions between native and introduced bees in New Zealand. New Zealand Journal of Ecology 3: 104–116.Google Scholar
  22. Donovan B.J., R.P. Macfarlane. (1984) Bees and Pollination, in: Scott R.R. (Ed.), New Zealand Pest and Beneficial Insects, Lincoln University of Agriculture, Christchurch, New Zealand, pp. 247–270.Google Scholar
  23. Eckert J.E. (1958) The Kangaroo Island Ligurian bees. Gleanings in Bee Culture 86: 660–663, 722–725.Google Scholar
  24. Estoup A., M. Solignac, M. Harry, J.M. Cornuet. (1993) Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nucleic Acids Research 21: 1427–1431.CrossRefGoogle Scholar
  25. Evanno G., S. Regnaut, J. Goudet. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefGoogle Scholar
  26. Franck P., L. Garnery, G. Celebrano, M. Solignac, J.M. Cornuet. (2000a) Hybrid origins of honeybees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Molecular Ecology 9: 907–921.CrossRefGoogle Scholar
  27. Franck P., L. Garnery, A. Loiseau, B.P. Oldroyd, H.R. Hepburn, et al. (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86: 420–430.CrossRefGoogle Scholar
  28. Franck P., L. Garnery, M. Solignac, J.M. Cornuet. (2000b) Molecular confirmation of a fourth lineage in honeybees from the Near East. Apidologie 31: 167–180.CrossRefGoogle Scholar
  29. Gallai N., J.M. Salles, J. Settele, B.E. Vaissière. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810–821.CrossRefGoogle Scholar
  30. Garnery L., J.M. Cornuet, M. Solignac. (1992) Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Molecular Ecology 1: 145–154.CrossRefGoogle Scholar
  31. Glatz R.V. (2015) Curious case of the Kangaroo Island honeybee Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) sanctuary. Austral Entomology 54: 117–126.CrossRefGoogle Scholar
  32. Government of South Australia. (1885) The Ligurian Bee Act - 1885. Government of South Australia, Adelaide, Australia.Google Scholar
  33. Gruber B., A. Adamack. (2017) PopGenReport: a simple framework to analyze population and landscape genetic data, Canberra, ACT, Australia.Google Scholar
  34. Han F., A. Wallberg, M.T. Webster. (2012) From where did the Western honeybee (Apis mellifera) originate?. Ecology and Evolution 2: 1949–1957.CrossRefGoogle Scholar
  35. Harpur B.A., S. Minaei, C.F. Kent, A. Zayed. (2012) Management increases genetic diversity of honey bees via admixture. Molecular Ecology 21: 4414–4421.CrossRefGoogle Scholar
  36. Hinson E.M., M. Duncan, J. Lim, J. Arundel, B.P. Oldroyd. (2015) The density of feral honey bee (Apis mellifera) colonies in South East Australia is greater in undisturbed than in disturbed habitats. Apidologie 46: 403–413.CrossRefGoogle Scholar
  37. Hopkins I. (1886) Illustrated Australasian Bee Manual. I. Hopkins, Auckland, New Zealand.Google Scholar
  38. Jolly B. (2004) South Australia’s early Ligurian beekeeping - and a lingering Kangaroo Island fable. Journal of the Historical Society of South Australia 32: 69–81.Google Scholar
  39. Jones O., J. Wang. (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10: 551–555.CrossRefGoogle Scholar
  40. Keogh R.C., A.P.W. Robinson, I.J. Mullins. (2010) Pollination aware: the real value of pollination in Australia, Rural Industries Research and Development Corporation, Canberra, ACT, Australia.Google Scholar
  41. Koulianos S., R. Crozier. (1996) Mitochondrial DNA sequence data provides further evidence that the honeybees of Kangaroo Island, Australia are of hybrid origin. Apidologie 27: 165–174.CrossRefGoogle Scholar
  42. Koulianos S., R. Crozier. (1997) Mitochondrial sequence characterisation of Australian commercial and feral honeybee strains, Apis mellifera L. (Hymenoptera: Apidae), in the context of the species worldwide. Australian Journal of Entomology 36: 359–363.CrossRefGoogle Scholar
  43. Lechner S., L. Ferretti, C. Schöning, W. Kinuthia, D. Willemsen, et al. (2014) Nucleotide variability at its limit? Insights into the number and evolutionary dynamics of the sex-determining specificities of the honey bee Apis mellifera. Molecular Biology and Evolution 31: 272–287.CrossRefGoogle Scholar
  44. Malfroy S.F., J.M.K. Roberts, S. Perrone, G. Maynard, N. Chapman. (2016) A pest and disease survey of the isolated Norfolk Island honey bee (Apis mellifera) population. Journal of Apicultural Research 55: 202–211.CrossRefGoogle Scholar
  45. Mattila H.R., T.D. Seeley. (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362–364.CrossRefGoogle Scholar
  46. Meixner M.D., M.A. Pinto, M. Bouga, P. Kryger, E. Ivanova, et al. (2013) Standard methods for characterising subspecies and ecotypes of Apis mellifera, in: Dietemann V., Ellis J.D., and Neumann P. (Eds.), The COLOSS BEEBOOK, Volume I: standard methods for Apis mellifera research. Journal of Apicultural Research 52, pp. IBRA. Scholar
  47. Murray W.E. (2001) The second wave of globalisation and agrarian change in the Pacific Islands. Journal of Rural Studies 17: 135–148.CrossRefGoogle Scholar
  48. Newstrom-Lloyd L.E. (2013) Pollination in New Zealand, Ecosystem services in New Zealand - conditions and trends, Manaaki Whenua Press, Lincoln, New Zealand.Google Scholar
  49. Oldroyd B.P. (1998) Controlling feral honey bee, Apis mellifera L. (Hymenoptera: Apidae), populations in Australia: methodologies and costs. Australian Journal of Entomology 37: 97–100.CrossRefGoogle Scholar
  50. Oldroyd B.P., J.M. Cornuet, D. Rowe, T.E. Rinderer, R.H. Crozier. (1995) Racial admixture of Apis mellifera in Tasmania, Australia: similaritites and differences with natural hybrid zones in Europe. Heredity 74: 315–325.CrossRefGoogle Scholar
  51. Oldroyd B.P., S.H. Lawler, R.H. Crozier. (1994) Do feral honey-bees (Apis mellifera) and regent parrots (Polytelis anthopeplus) compete for nest sites. Australian Journal of Ecology 19: 444–450.CrossRefGoogle Scholar
  52. Oldroyd B.P., W.S. Sheppard, J.A. Stelzer. (1992) Genetic characterization of the bees of Kangaroo Island, South Australia. Journal of Apicultural Research 31: 141–148.CrossRefGoogle Scholar
  53. Oldroyd B.P., E.G. Thexton, S.H. Lawler, R.H. Crozier. (1997) Population demography of Australian feral bees (Apis mellifera). Oecologia 111: 381–387.CrossRefGoogle Scholar
  54. Oxley P.R., B.P. Oldroyd. (2009) Mitochondrial sequencing reveals five separate origins of ‘Black’ Apis mellifera (Hymenoptera: Apidae) in Eastern Australian commercial colonies. Journal of Economic Entomology 102: 480–484.CrossRefGoogle Scholar
  55. Piry S., G. Luikart, J.M. Cornuet. (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502–503.CrossRefGoogle Scholar
  56. Pritchard J.K., M. Stephens, P. Donnelly. (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  57. R Development Core Team. (2017) R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  58. Raymond M., F. Rousset. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.CrossRefGoogle Scholar
  59. Remnant E.J., M. Shi, G. Buchmann, T. Blaquiere, E.C. Holmes, et al. (2017) A diverse range of novel RNA viruses in geographically distinct honey bee populations. Journal of Virology 91: 16.Google Scholar
  60. Roberts J., D. Anderson, P. Durr. (2015) Upgrading knowledge on pathogens (particularly viruses) of Australian honey bees, Rural Industries Research and Development Corporation, Canberra, Australia.Google Scholar
  61. Ruttner F. (1976) Isolated populations of honeybee in Australia. Journal of Apicultural Research 15: 97–104.CrossRefGoogle Scholar
  62. Ruttner F. (1988) Biogeography and Taxonomy of Honeybees. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
  63. Seeley T.D. (1985) Honeybee Ecology: A Study of Adaptation in Social Life. Princeton University Press, Princeton, New Jersey, USA.Google Scholar
  64. Solignac M., D. Vautrin, A. Loiseau, F. Mougel, E. Baudry, et al. (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Molecular Ecology Notes 3: 307–311.CrossRefGoogle Scholar
  65. Solorzano C.D., A.L. Szalanski, M. Kence, J.A. McKern, J.W. Austin, et al. (2009) Phylogeography and population genetics of honey bees (Apis mellifera) from Turkey based on COI-COII sequence data. Sociobiology 53: 237–246.Google Scholar
  66. Tarpy D.R., R.E. Page. (2002) Sex determination and the evolution of polyandry in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 52: 143–150.CrossRefGoogle Scholar
  67. Tarpy D.R., D. vanEngelsdorp, J.S. Pettis. (2013) Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften 100: 723–728.CrossRefGoogle Scholar
  68. Uzunov A., C. Costa, B. Panasiuk, M. Meixner, P. Kryger, et al. (2014) Swarming, defensive and hygenic behaviour in honey bee colonies of different genetic origin in a pan-European experiment. Journal of Apicultural Research 53: 248–260.CrossRefGoogle Scholar
  69. van der Velde M., S.R. Green, M. Vanclooster, B.E. Clothier. (2007) Sustainable development in small island developing states: agricultural intensification, economic development, and freshwater resources management on the coral atoll of Tongatapu. Ecological Economics 61: 456–468.CrossRefGoogle Scholar
  70. van Oosterhout C., W.F. Hutchinson, D.P.M. Wills, P. Shipley. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  71. vanEngelsdorp D., J. Hayes, R.M. Underwood, J. Pettis. (2008) A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PLoS One 3: e4071.CrossRefGoogle Scholar
  72. Weatherhead T. (1986) Boxes to Bar Hives: Beekeeping History or Queensland. International Colour Productions, Stanthorpe, QLD, Australia.Google Scholar
  73. White B., E. Remnant, L. Osborne. (2016) Beekeeping in the Kingdom of Tonga. Honeybee News 9: 34–38.Google Scholar
  74. Whitfield C.W., S.K. Behura, S.H. Berlocher, A.G. Clark, J.S. Johnston, et al. (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 643–645.CrossRefGoogle Scholar
  75. Winston M.L. (1987) The Biology of the Honey Bee. Harvard University Press, Cambridge, MA, USA.Google Scholar
  76. Woodward D. (1993) Ligurian bees. American Bee Journal 133: 124–125.Google Scholar
  77. Woyke J. (1963) What happens to diploid drone larvae in a honeybee colony? Journal of Apicultural Research 2: 73–75.CrossRefGoogle Scholar
  78. Woyke J. (1976) Population genetic studies on sex alleles in the honeybee using the example of the Kangaroo Island bee sanctuary. Journal of Apicultural Research 15: 105–123.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  • Nadine C. Chapman
    • 1
  • Jiani Sheng
    • 1
  • Julianne Lim
    • 1
  • Samuel F. Malfroy
    • 2
  • Brock A. Harpur
    • 3
    • 4
  • Amro Zayed
    • 3
  • Michael H. Allsopp
    • 5
  • Thomas E. Rinderer
    • 6
  • John M. K. Roberts
    • 7
  • Emily J. Remnant
    • 1
  • Benjamin P. Oldroyd
    • 1
  1. 1.School of Life and Environmental Science, Behaviour and Genetics of Social Insects LaboratoryUniversity of SydneySydneyAustralia
  2. 2.Australian Government Department of Agriculture and Water ResourcesCanberraAustralia
  3. 3.Department of BiologyYork UniversityTorontoCanada
  4. 4.Donnelly Centre for Cellular and Biomolecular ResearchUniversity of TorontoTorontoCanada
  5. 5.ARC-Plant Protection Research InstituteStellenboschSouth Africa
  6. 6.Honey Bee Breeding, Genetics and Physiology Research LaboratoryUSDA-ARSBaton RougeUSA
  7. 7.Health and Biosecurity, Commonwealth Scientific and Industrial Research OrganisationBlack MountainAustralia

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