Geometric Morphometric Analysis of Forewings of Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) Populations in Thailand
Keywords:
Apis mellifera, forewing, geometric morphometrics, landmark, ThailandAbstract
Apis mellifera beekeeping in Thailand started in the 1970s and since then has spread throughout the country. There is little information on diversity, especially morphological diversity, of these species in Thailand. The objective of this study was to examine variation among A. mellifera populations in Thailand based on geometric morphometrics of forewings. We collected A. mellifera worker bees of 160 colonies from 25 apiaries throughout Thailand. Forewing shape variation was examined based on 19 landmark coordinates. The results showed high wing morphological variation. Apis mellifera samples from Thailand were found to belong to 5 distinct groups, which were further supported by a hierarchical cluster analysis. In the size analysis, the honey bees in 5 morphotypes differed significantly in wing centroid size (p < 0.0001). Canonical variate analysis (CVA) revealed 5 distinct groups with significance in all groups (P < 0.001), and a high rate of correct classification based on a cross-validation test (85.63%) was found. Our study provided information on morphological diversity of A. mellifera in Thailand and asserts that forewing geometric morphometrics is a simple, reliable, inexpensive method that is sufficient for determination of morphological diversity of this species.
References
Abou-Shaara, H.F. and Al-Ghamdi, A.A. 2012. Studies on wings symmetry and honey bee races discrimination by using standard and geometric morphometrics. Biotechnology in Animal Husbandry, 28(3): 575-584.
Alburaki, M., Bertrand, B., Legout, H., Moulin, S., Alburaki, A., Sheppard, W.S. and Garnery, L. 2013. A fifth major genetic group among honeybees revealed in Syria. BMC Genetics, 14(1): 117-127.
Arias, M.C., Rinderer, T.E. and Sheppard, W.S. 2006. Further characterization of honeybees from the Iberian Peninsula by allozyme, morphometric and mtDNA haplotype analyses. Journal of Apicultural Research, 45(4): 188-196.
Arnqvist, G. and Martensson, T. 1998. Measurement error in geometric morphometrics: empirical strategies to assess and reduce its impact on measurements of shape. Acta Zoologica Academiae Scientiarum Hungaricae, 44(1): 73-96.
Aytekin, A.M., Terzo, M., Rasmont, P. and Cagatay, N. 2007. Landmark based geometric morphometric analysis of wing shape in Sibricobombus Vogt (Hymenoptera: Apidae: Bombusi Latrielle). Annales- Societe Entomologique de France, 43(1): 95-102.
Barour, C., Tahar, A. and Baylac, M. 2011. Forewing shape variation in Algerian honey bee population of Apis mellifera intermissa (Buttel-Reepen, 1906) (Hymenoptera: Apidae): A landmark-based geometric morphometric analysis. African Entomology, 19(1): 11-22.
Barour, C. and Baylac, M. 2016. Geometric morphometric discrimination of the three African honeybee subspecies Apis mellifera intermissa, A. m. sahariensis and A. m. capensis (Hymenoptera: Apidae): Fore wing and hind wing landmark configurations. Journal of Hymenoptera Research, 52(52): 61-70.
Bodur, C., Kence, M. and Kence, A. 2007. Genetic structure of honeybee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46(1): 50-56.
Bonatti, V., Simões, Z.L.P., Franco, F.F. and Francoy, T.M. 2014. Evidence of at least two evolutionary lineages in Melipona subnitida (Apidae, Meliponini) suggested by mtDNA variability and geometric morphometrics of forewings. Naturwissenschaften, 101(1): 17-24.
Bookstein, F.L. 1991. Morphometric tools for landmark data. In Geometry and Biology. Cambridge University Press, United Kingdom, 455 pp.
Bouga, M. and Hatjina, F. 2005. Genetic variability in Greek honey bee (A. mellifera L.) populations using geometric morphometric analyses. Proceedings of The Balkan Scientific Conference of Biology, Plovdiv, Bulgaria, 19-21 May 2005. Plovdiv University Press, Plovdiv, Bulgaria. 598-602.
Bouga, M., Alaux, C., Bienkowska, M., Büchler, R., Carreck, N.L., et al. 2011. A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50(1): 51-84.
Chantawannakul, P. 2018. Bee diversity and current status of beekeeping in Thailand. In: Chantawannakul, P., Williams, G. and Neumann, P. (Eds). Asian beekeeping in the 21st century, Springer, Singapore. pp. 269-285.
Charistos, L., Hatjina, F., Bouga, M., Mladenovic, M. and Maistros, A.D. 2014. Morphological discrimination of Greek honey bee populations based on geometric morphometrics analysis of wing shape. Journal of Apicultural Science, 58(1): 75-84.
De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I. and Serrano, J. 2009. Biodiversity, conservation and current threats to European honeybees. Apidologie, 40(3): 263-284.
de Souza, A.L.D.S., Multini, L.C., Marrelli, M.T. and Wilke, A.B.B. 2020. Wing geometric morphometrics for identification of mosquito species (Diptera: Culicidae) of neglected epidemiological importance. Acta Tropica, 211(p. e105593).
Dolati L, Rafi, J.N. and Khalesro, H. 2013. Landmark-based morphometric study in the fore and hind wings of an Iranian race of European honeybee (Apis mellifera meda). Journal of Apicultural Science, 57(2): 187-197.
Dryden, I.L. and Mardia, K.V. 1998. Statistical Shape Analysis. John Wiley and Sons, New York, 347 pp.
Dujardin, J.P. 2008. Morphometrics applied to medical entomology. Infection, Genetics and Evolution, 8(6): 875-890.
Engel, M. S. 1999. The Taxonomy of Recent and Fossil Honey Bees (Hymenoptera: Apidae; Apis). Journal of Hymenoptera Research, 8(2): 165-196.
Falamarzi, S., Habibpour, B., Mossadegh, M.S. and Monfared, A. 2016. Differentiation of five species of Megachile (Hymenotera: Megachilidae), based on wing shape. Journal of Apicultural Science, 60(2): 41-50.
Francisco, F.O., Nunes-Silva, P., Francoy, T.M., Wittmann, D., Imperatriz-Fonseca, V.L., Arias, M.C. and Morgan, E.D. 2008. Morphometric, biochemical and molecular tools for assessing biodiversity: an example in Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Insects Sociaux, 55(3): 231-237.
Franck, P., Garnery, L., Solignac, M. and Cornuet, J.M. 1998. The origin of west European subspecies of honeybees (Apis mellifera): New insights from microsatellite and mitochondrial data. Evolution, 52(4): 1119-1134.
Franck, P., Garnery, L., Loiseau, A., Oldroyd, B.P., Hepburn, H.R., Solignac, M. and Cornuet, J.M. 2001. Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity, 86(Pt4): 420-430.
Francoy, T.M., Prodo, P.R.R., Gonçalves, L.S., Costa, L.D. and de Jong, D. 2006. Morphometric differences in a single wing cell can discriminate Apis mellifera racial types. Apidologie, 37(1): 91-97.
Francoy, T.M., Wittmann, D., Drauschke, M., Muller, S., Steinhage, V., Bezerra-Laure, M.A.F., De Jong, D. and Goncalves, L.S. 2008. Identification of Africanized honey bees through wing morphometrics: two fast and efficient procedures. Apidologie, 39(5): 488-494.
Francoy, T.M., Silva, R.A.O., Nunes-Silva, P., Menezes, C. and Imperatriz-Fonseca, V.L. 2009. Gender identification of five genera of stingless bees (Apidae, Meliponini) based on wing morphometry. Genetics and Molecular Research, 8(1): 207-214.
Francoy, T.M., Grassi, M.L., Imperatriz-Fonseca, V.L., de Jesús May-Itzá, W. and Quezada-Euán, J. J.G. 2011. Geometric morphometrics of the wing as a tool for assigning genetic lineages and geographic origin to Melipona beecheii (Hymenoptera: Meliponini). Apidologie, 42(4): 499-507.
Francoy, T. M., Franco, F.D.F. and Roubik, D.W. 2012. Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie, 43(6): 609-617.
Garnery, L., Solignac, M., Celebrano, G. and Cornuet, J.M. 1993. A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia, 49(11): 1016-1021.
Gruber, K., Schöning, C., Otte, M., Kinuthia, W. and Hasselmann, M. 2013. Distinct subspecies or phenotypic plasticity? Genetic and morphological differentiation of mountain honey bees in East Africa. Ecology and Evolution, 3(10): 3204-3218.
Gumiel, M., Catalá, S., Noireau, F., Rojas De Arias, A., García, A. and Dujardin, J.P. 2003. Wing geometry in Triatoma infestans (Klug) and T. melanosoma Martinez, Olmedo & Carcavallo (Hemiptera: Reduviidae). Systematic Entomology, 28(2): 173-180.
Hammer, Ø., Harper, D.A.T. and Ryan, P.D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1): 1-9.
Henriques, D., Chavez-Galarza, J., Teixeira, J. S.G., Ferreira, H., Neves, C.J., Francoy, T. M. and Pinto, M.A. 2020. Wing geometric morphometrics of workers and drones and single nucleotide polymorphisms provide similar genetic structure in the Iberian honey bee (Apis mellifera iberiensis). Insects, 11(2): 1-14.
Ilyasov, R.A., Kutuev, I.A., Petukhov, A.V., Poskryakov, A.V. and Nikolenko, A.G. 2011. Phylogenetic relationships of dark European honeybees Apis mellifera mellifera L. from the Russian Ural and West European populations. Journal of Apicultural Science, 55(1): 67-76.
Janczyk, A. and Tofilski, A. 2021. Monthly changes in honey bee forewings estimated using geometric morphometrics. Journal of Apicultural Science, 65(1): 139-146.
Jensen, A.B., Palmer, K.A., Boomsma, J.J. and Pedersen, B.V. 2005. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, 14(1): 93-106.
Kandemir, İ., Özkan, A. and Fuchs, S. 2011. Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach. Apidologie, 42(5): 618-627.
Kavinseksan, B., Wongsiri, S., Rinderer, T.E. and De Guzman, L.I. 2004. Comparison of the hygienic behavior of ARS Russian commercial honey bees in Thailand. American Bee Journal, 144(11): 870-872.
Kekecoglu, M., Bouga, M., Soysal, M.I. and Harizanis, P. 2007. Morphometrics as a tool for the study of genetic variability of honey bees. Journal of Tekirdag Agricultural Faculty, 4(1): 7-15.
Klingenberg, C.P. 2011. MORPHO J: an integrated software package for geometric Morphometrics. Molecular Ecology Resources, 11(2): 353-357.
Klingenberg, C.P. and Mclntyre, G.S. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52(5): 1363-1375.
Kükrer, M., Kence, M. and Kence, A. 2021. Honey bee diversity is swayed by migratory beekeeping and trade despite conservation practices: genetic evidences for the impact of anthropogenic factors on population structure. Frontiers in Ecology and Evolution, 9: 556-816.
Miguel, I., Baylac, M., Iriondo, M., Manzano, C., Garnery, L. and Estonba, A. 2011. Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie, 42(2): 150-161.
Moritz, R.F.A., Härtel, S. and Neumann, P. 2005. Global invasions of the western honey bee (Apis mellifera) and the consequences for biodiversity. Ecoscience, 12(3): 289-301.
Nawrocka, A., Kandemir, I., Fuchs, S. and Tofilski, A. 2018. Computer software for identification of honey bee subspecies and evolutionary lineage. Apidologie, 49(2): 172-184.
Nedic, N., Jevtic, G., Jez, G., Andelkovic, B., Milosavljevic, S. and Kostic, M. 2011. Forewing differentiation of the honey bees from Serbia. Biotechnology in Animal Husbandry, 27(3): 1387-1394.
Neumann, P., Moritz, R.F.A. and Van Praagh, J. 1999. Queen mating frequency in different types of honey bee mating apiaries. Journal of Apicultural Research, 38(1-2): 11-18.
Nürnberger, F., Härtel, S. and Steffan-Dewenter, I. 2019. Seasonal timing in honey bee colonies: phenology shifts affect honey stores and varroa infestation levels. Oecologia, 189(4): 1121-1131.
Oleksa, A. and Tofilski, A. 2015. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of honey bee subspecies. Apidologie, 46(1): 49-60.
Palmer, K. and Oldroyd, B.P. 2000. Evolution of multiple mating in the genus Apis. Apidologie, 31(2): 235-248.
Porrini, L.P., Quintana, S., Brasesco, C., Porrini, M.P., Garrido, P.M., Eguaras, M.J., Müller, F. and Iriarte, P.F. 2019. Southern limit of Africanized honey bees in Argentina inferred by mtDNA and wing geometric morphometric analysis. Journal of Apicultural Research, 59(4): 1-10.
Raina, S.K. and Kimbu, D.M. 2005. Variations in races of the honeybee Apis mellifera (Hymenoptera: Apidae) in Kenya. International Journal of Tropical Insect Science, 25(4): 281-291.
Raina, S. K., Kioko, E., Zethner, O. and Wren, S. 2011. Forest habitat conservation in Africa using commercially important insects. Annual Review of Entomology, 56(1): 465-485.
Rattanawannee, A., Chanchao C. and Wongsiri S. 2010. Gender and species identification of four native honey bees (Apidae: Apis) in Thailand based on wing morphometic analysis. Annals of the Entomological Society of America, 103(6): 965-970.
Rattanawannee, A., Chanchao, C. and Wongsiri, S. 2012. Geometric morphometric analysis of giant honeybee (Apis dorsata Fabricius, 1793) populations in Thailand. Journal of Asia- Pacific Entomology, 15(4): 611-618.
Rattanawannee, A., Duangphakdee, O., Chanchao, C., Teerapakpinyo, C., Warrit, N., Wongsiri, S. and Oldroyd, B.P. 2019. Genetic characterization of exotic commercial honey bee (Hymenoptera: Apidae) populations in Thailand reveals high genetic diversity and low population substructure. Journal of Economic Entomology, 113(1): 34-42.
Rizwan, M., Li, Z., Nie, H., Qasim, M., Raza, M., Kalan, A., Tayyab, M. and Su, S. 2018. High mitochondrial diversity of Apis mellifera under COI gene from China and Pakistan. Applied Ecology and Environmental Research, 13(6): 2933-2945.
Ruttner, F. 1988. Biogeography and Taxonomy of Honeybees, Springer Verlag, Berlin, 284 pp.
Rohlf, F.J. 2015. The tps series of software. Hystrix, the Italian Journal of Mammalogy, 26(1): 9-12.
Seeley, T.D. 1985. Honeybee ecology: a study of adaptation in social life. Princeton University Press, Princeton, 214 pp.
Shaibi, T., Fuchs, S. and Moritz, R.F.A. 2009. Morphological study of honeybees (Apis mellifera) from Libya. Apidologie, 40(2): 97-105.
Slice, D.E. 2007. Geometric morphometrics. Annual Review Anthropology, 36(1): 261-281.
Suppasat, T., Smith, D.R., Deowanish, S. and Wongsiri, S. 2007. Matrilineal origins of Apis mellifera in Thailand. Apidologie, 38(4): 323-334.
Tofilski, A. 2008. Using geometric morphometrics and standard morphometry to discriminate three honey bee subspecies. Apidologie, 39(5): 558-563.
Villemant, C., Simbolotti, G. and Kenis, M. (2007). Discrimination of Eubazus (Hymenoptera, Braconidae) sibling species using geometric morphometrics analysis of wing venation. Systematic Entomology, 32(4): 625-634.
Wȩgrzynowicz, P., Gerula, D., Tofilski, A., Panasiuk, B. and Bieńkowska, M. 2019. Maternal inheritance in hybrids of three honey bee subspecies. Journal of Apicultural Science, 63(1): 131-138.
Whitfield, C.W., Behura, S.K., Berlocher, S.H., Clark, A.G., Johnston, J.S., Sheppard, W.S., Smith, D.R., Suarez, A.V., Weaver, D. and Tsutsui, N.D. 2006. Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science, 314(5799): 642-645.
Wongsiri, S., Chanchao, C., Deowanish, S., Aemprapa, S., Chaiyawong, T., Peterson, S. and Leepitakrat, S. 2000. Honeybee diversity and beekeeping in Thailand. Bee World, 81(1): 20-29.
Zhou, S., Zhu, X., Xu, X., Zheng, X. and Zhou, B. 2016. Assessing of geometric morphometrics analyses in microtaxonomy of the Apis cerana Fabricius (Hymenoptera: Apidae) within China. Journal of the Kansas Entomological Society, 89(4): 297-305.
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