279
Views
2
CrossRef citations to date
0
Altmetric
Evolution, Phylogeny, and Biogeography

Mitochondrial DNA (mtDNA) markers reveal low genetic variation and the presence of two honey bee races in Uganda’s agro-ecological zones

Marcadores de ADN mitocondrial (mtDNA) revelan una baja variación genética y presencia de dos razas de abeja de la miel en las zonas agroecológicas de Uganda

, , , , , & show all
Pages 112-121 | Received 16 Aug 2016, Accepted 20 Jan 2017, Published online: 15 Mar 2017

References

  • Achou, M., Loucif-ayad, W., Legout, H., Hmidan, H., Alburaki, M., & Garnery, L. (2015) An insightful molecular analysis reveals foreign honey bees among Algerian honey bee populations (Apis mellifera L.). Data Mining in Genomics & Proteomics, 6, 6–11.
  • Afik, O., Dag, A., Yeselson, Y., Schaffer, A., & Shafir, S. (2010). Selection and breeding of honey bees for higher or lower collection of avocado nectar. Journal of Economic Entomology, 103, 228–233.10.1603/EC09235
  • Alburaki, M., Moulin, S., Legout, H., Alburaki, A., & Garnery, L. (2011). Mitochondrial structure of Eastern honey bee populations from Syria, Lebanon and Iraq. Apidologie, 42, 628–641.10.1007/s13592-011-0062-4
  • Arias, M.C., Brito, R.M., Flávio de Oliveira, F., Moretto, G., De Oliveira, F.F., Silvestre, D., & Sheppard, W.S. (2006). Molecular markers as a tool for population and evolutionary studies of stingless bees. Apidologie, 37, 1–16.
  • Arturo, J., & Segura, L. (2000). Highly polymorphic DNA markers in an Africanized honey bee population in Costa Rica. Genetics and Molecular Biology, 322, 317–322.
  • Barour, C., Tahar, A., & Baylac, M. (2011). Forewing shape variation in Algerian honey bee populations of Apis mellifera intermissa (Buttel-Reepen, 1906) (Hymenoptera: Apidae): A landmark-based geometric morphometrics analysis. African Entomology, 19, 11–22.10.4001/003.019.0101
  • Batra, S.W.T. (1995). Bees and pollination in our changing environment. Apidologie, 26, 361–370.10.1051/apido:19950501
  • Chahbar, N., Muñoz, I., & Dall’Olio, R., De la Rúa, P., Serrano, J., & Doumandji, S. (2013). Population structure of North African honey bees is influenced by both biological and anthropogenic factors. Journal of Insect Conservation, 17, 385–392.10.1007/s10841-012-9520-1
  • Charistos, L., Hatjina, F., Bouga, M., Mladenovic, M., & Maistros, A.D. (2014). Morphological discrimination of greek honey bee populations based on geometric morphometric analysis of wing shape. Journal of Apicultural Science, 58, 75–84.
  • Clement, M., Posada, D., & Crandall, K.A. (2000). TCS: A computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.10.1046/j.1365-294x.2000.01020.x
  • Corander, J., & Tang, J. (2007). Bayesian analysis of population structure based on linked molecular information. Mathematical Biosciences, 205, 19–31.10.1016/j.mbs.2006.09.015
  • Cornuet, J.-M., & Garnery, L. (1991). Mitochondrial DNA variability in honey bees and its phylogeographic implications. Apidologie, 22, 627–642.10.1051/apido:19910606
  • Cornuet, J.-M., Garnery, L., & Solignac, M. (1991). Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics, 1128, 393–403.
  • De La Rúa, P., Galián, J., Serrano, J., & Moritz, R.F.A. (2001). Genetic structure and distinctness of Apis mellifera L. populations from the Canary Islands. Molecular Ecology, 10, 1733–1742.10.1046/j.1365-294X.2001.01303.x
  • Eisa, M.A., & Roth, M. (2008). Overview of traditional beekeeping in Sudan (pp. 1–5). In Competition for resources in a changing world: New drive for rural development. Hohenheim.
  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver 3.0 – An integrated software package for population genetics. Evolutionary Bioinformatics Online, 1, 47–50.
  • Excoffier, L., Smouse, P.E., & Quattro, J.M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics Society of America, 491, 479–491.
  • Franck, P., Garnery, L., Loiseau, A., Oldroyd, B.P., Hepburn, H.R., Solignac, M., & Cornuet, J.M. (2001). Genetic diversity of the honey bee in Africa: Microsatellite and mitochondrial data. Heredity, 86, 420–430.10.1046/j.1365-2540.2001.00842.x
  • Francoy, T.M., Wittmann, D., Drauschke, M., Müller, S., Steinhage, V., Bezerra-Laure, M.A.F., … Goncalves, L.S. (2008). Identification of Africanized honey bees through wing morphometrics: Two fast and efficient procedures. Apidologie, 39, 488–494.10.1051/apido:2008028
  • Garnery, L., Cornuet, J.M., & Solignac, M. (1992). Evolutionary history of the honey bee Apis mellifera infered from mitochondrial DNA analysis. Molecular Ecology, 1, 145–154.10.1111/j.1365-294X.1992.tb00170.x
  • Garnery, L., Vautrin, D., Cornuet, J.-M., & Solignac, M. (1991). Phylogenetic relationships in the genus Apis inferred from mitochondrial DNA sequence data. Apidologie, 22, 87–92.10.1051/apido:19910111
  • Haddad, N., Meixner, M.D., Fachs, S., Migdadi, H., Garnery, L., & Sheppard, W.S. (2009). Mitochondrial DNA support for genetic reserves of Apis mellifera syriaca in Jordan. Journal of Apicultural Research and Bee World, 1, 19–22.
  • Hall, G.H., Zettel-Nalen, C., & Ellis, J.D. (2005). African honey bee: What you need to know. Florida: University of Florida, IFAS Extension.
  • Hepburn, H.R. & Radloff, S.E. (1998). Honey bees of Africa. Berlin Heidelberg GmbH: Springer-Verlag.10.1007/978-3-662-03604-4
  • Hepburn, H.R., Radloff, S.E., & Oghiakhe, S. (2000). Mountain honey bees of Africa. Apidologie, 31, 205–221.10.1051/apido:2000117
  • Ilyasov, R.A., Kutuev, L.A., Poskryakov, A.V., Petukhov, A.V., & Nikolenko, A.G. (2011). Phylogenetic relationships of dark European honey bees Apis mellifera mellifera L. from the Russian ural and west European populations. Journal of Apicultural Science, 55, 67–77.
  • Ivanova, E.N., Petrov, P., Bouga, M., Emmanoue, N.G., Tunca, R.I., & Kence, M. (2010). Genetic variation in honey bee (Apis mellifera L.) populations from Bulgaria. Journal of Apicultural Science, 54, 51–62.
  • Kajobe, R., Kato, E.K., Otim, S.A., Kasangaki, P., & Abila, P.P. (2016). Status of honey bee pests in Uganda. Bulletin of Animal Health and Production in Africa Bee, 2016, 105–117.
  • Kajobe, R., Marris, G., Budge, G., Laurenson, L., Cordoni, G., Jones, B., … Brown, M.A. (2010). First molecular detection of a viral pathogen in Ugandan honey bees. Journal of Invertebrate Pathology, 104, 153–156.10.1016/j.jip.2010.02.007
  • Kajobe, R., Agea, J.G., Kugonza, D.R., Alioni, V., Otim, S.A., Rureba, T., & Marris, G. (2009). National beekeeping calendar, honey bee pest and disease control methods for improved production of honey and other hive products in Uganda. Entebbe, Uganda: NARO.
  • Kajobe, R. (2008). Foraging behaviour of equatorial Afrotropical stingless bees: habitat selection and competition for resources, Sephine Enterprises (U).
  • Kamrani, B., Pirany, N., Hashemi, A., & Kamrani, M. (2012). Genetic characterization of honey bees (Hymenoptera : Apidea) populations from north west of Iran using RAPD markers. Technical Journal of Engineering and Applied Sciences, 2, 430–435.
  • Kasangaki, P., Otim, A.S., Abila, P.P., Angiro, C., Chemurot, M., & Kajobe, R. (2015). The presence of varroa in Uganda and knowledge about it by the beekeeping industry. Journal of Apicultural Research, 54, 373–377. doi:10.1080/00218839.2016.1159858.
  • Landau, S., & Everitt, B.S. (2004). A handbook of statistical analyses using SPSS. Chapman & Hall/CRC A.
  • Lee, J.Y., Wang, R.A., Cho, Y.S., Thapa, R., Kwon, H.W., & Kim, I. (2016). Original article mitochondrial DNA variations in Korean Apis cerana (Hymenoptera: Apidae) and development of another potential marker. Apidologie, 47, 123–134.
  • MAAIF, UBOS. (2010). The national livestock census report 2008. Uganda: Kampala.
  • Meixner, M.D., Pinto, M.A., Bouga, M., Kryger, P., Ivanova, E., & Fuchs, S. (2013). Standard methods for characterising subspecies and ecotypes of Apis mellifera. In V. Dietemann, J.D. Ellis, & P. Neumann (Eds.), The COLOSS BEEBOOK, Volume I: standard methods for Apis mellifera research. Journal of Apicultural Research, 52(4), 1–28. doi:10.3896/IBRA.1.52.4.05
  • Moritz, R.F.A., Cornuet, J.-M., Kryger, P., Garnery, L., & Hepburn, H.R. (1994). Mitochondrial DNA variability in South African honey bees (Apis mellifera L). Apidologie, 25, 169–178.10.1051/apido:19940205
  • Nei, M. (1987). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.
  • Nei, M., & Miller, J.C. (1990). A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics, 125, 873–879.
  • Parks, D.H., Porter, M., Churcher, S., Wang, S., Blouin, C., Whalley, J., … Beiko, R.G. (2009). GenGIS: A geospatial information system for genomic data. Genome Research, 1–10.
  • Pinto, M.A., Henriques, D., Chávez-Galarza, J., Kryger, P., Garnery, L., van der Zee, R., … Johnston, J.S. (2014). Genetic integrity of the dark European honey bee (Apis mellifera mellifera) from protected populations: a genome-wide assessment using SNPs and mtDNA sequence data. Journal of Apicultural Research, 53, 269–278. doi:10.3896/IBRA.1.53.2.08.
  • Radloff, S., & Hepburn, R. (2000). Population structure and morphometric variance of the Apis mellifera scutellata group of honey bees in Africa. Genetics and Molecular Biology, 23, 305–316.10.1590/S1415-47572000000200012
  • Raina, S.K., & Kimbu, D.M. (2005). Variations in races of the honey bee Apis mellifera (Hymenoptera: Apidae) in Kenya. International Journal of Tropical Insect Science, 25, 281–291.
  • Roe, A.H. (2000). Africanized Honey Bee. Logan, USA: Utah State University Extension.
  • Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X., & Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497.10.1093/bioinformatics/btg359
  • Ruttner, F. (1971) Morphological and biological characterization of economically interesting bee. Apiacta, 4.
  • Ruttner, F., Kauhausen, D., & Koeniger, N. (1989). Position of the red honey bee, Apis koschevnikovi (Buttel-Reepen 1906), within the Genus Apis. Apidologie, 20, 395–404.10.1051/apido:19890504
  • Segeren, P. (2004). Beekeeping in the tropics (5th ed.). Wageningen, Netherlands: Agromisa Foundation.
  • Shao, Z., Mao, H., Ono, M., Wang, D.S., Bonizzoni, M., & Zhang, Y.-P. (2004). Genetic structure of Asian populations of Bombus ignitus (Hymenoptera: Apidae). Journal of Heredity, 95, 46–52.10.1093/jhered/esh008
  • Sheppard, W.S., Arias, M.C., Grech, A., & Meixner, M.D. (1997). Apis mellifera ruttneri, a new honey bee subspecies from Malta. Apidologie, 28, 287–293.10.1051/apido:19970505
  • Tan, K., Qu, Y., Wang, Z., Liu, Z., & Engel, M.S. (2016). Haplotype diversity and genetic similarity among populations of the Eastern honey bee from Himalaya- Southwest China and Nepal (Hymenoptera: Apidae). Apidologie, 47, 197–205.
  • Tan, K., Warrit, N., & Smith, D.R. (2007). Mitochondrial DNA diversity of Chinese Apis cerana. Apidologie, 38, 238–246.10.1051/apido:2007008
  • Techer, M.A., Clémencet, J., Turpin, P., Volbert, N., Reynaud, B., & Delatte, H. (2015). Genetic characterization of the honey bee (Apis mellifera) population of Rodrigues Island, based on microsatellite and mitochondrial DNA. Apidologie, 46, 445–454.
  • Thompson, J.D., Higgins, D.G., & Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.10.1093/nar/22.22.4673
  • Tunca, R.I., & Kence, M. (2011). Genetic diversity of honey bee (Apis mellifera L.: Hymenoptera: Apidae) populations in Turkey revealed by RAPD markers. African Journal of Agricultural Research, 6, 6217–6225.
  • UEPB and the sector counterpart team (2005). Uganda apiculture export strategy. Uganda: Kampala.
  • Yin, L., & Ji, T. (2013). Genetic diversity of the honey bee Apis cerana in Yunnan, China, based on mitochondrial DNA. Genetics and Molecular Research, 12, 2002–2009.10.4238/2013.June.20.1

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.