Morphological wing templates of drone bees for populations of Apis mellifera in Ukraine
Abstract
The testing of morphometric templates (standards) for drone wings, obtained from previous studies of bees in Lviv, Zhytomyr, Kyiv, Sumy, Kharkiv, and Poltava regions of Ukraine, was conducted to assess their suit a bility for determining the subspecies and population affiliation of colonies from local honey bee populations. For this purpose, 1 , 492 drone wings from 14 colonies of a breeding apiary in the Khmelnytskyi region were classified into four clusters based on eight indices: Ci, Dbi, Pci, Disc. sh., Ri (traditional), and Ci.3, Ci.2.1, Ci.2.2 (proposed by the authors). Cluster identification was carried out using morphometric templates: "Car nica", representing a local population of the subspecies A. m. carnica ; "UkrBee" – Ukrainian bees; "UkrStep" – Ukrainian steppe bees (for which subspecies identification has not been reliably established); and "HybrCaucas" – a probable hybrid of the subspecies A. m. caucasica , based on Mahalanobis distances between the centroids of templates and clusters. It was established that four populations of honey bees predominate at the location of the apiary. At the next stage of the study, a classification of 1 , 939 drone wings into two clusters was performed for each of the 22 colonies (an additional 8 colonies were included for further analysis). The identification of phenotypes for each of the clusters was carried out in a similar manner by comparison with the aforementioned templates. This made it possible to identify the subspecies and population affiliation of wing phenotypes for 28 (65%) clusters. The results of identifying subspecies and population affiliation of drone wing phenotypes using templates derived within the framework of classical morphometrics indicate the effectiveness of the applied methodology and can be used for the preliminary assessment of the probable genomic compos i tion of drones and queens in the part related to wing morphology. In addition to its primary objective, this study expands knowledge about the racial composition of honey bees in Ukraine. The obtained information on the probable genomic composition of queens can be applied in breeding programs to increase the presence of desired populations at a given apiary and to eliminate populations or hybrids whose presence is undesirable.References
Alaux, C., Le Conte, Y., & Decourtye, A. (2019). Pitting wild bees against managed honey bees in their native range, a losing strategy for the conservation of honey bee biodiversity. Frontiers in Ecology and Evolution, 7, 60.
Albarrak, A. B., & Gray, A. (2023). Seasonal colony loss rates and honey bee management in the kingdom of Saudi Arabia: Results of a survey of beekeepers. Insects, 14(6), 513.
Anderson, D. L., & Trueman, J. W. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24(3), 165–189.
Babenko, V. V., Cherevatov, O. V., & Yarovets, V. I. (2024b). Variability of wing morphology of Apis mellifera in Ukraine. Agrology, 7(4), 144–153.
Babenko, V. V., Galatiuk, O. E., & Yarovets, V. I. (2024a) Utochneni morfometrychni etalony kryl trutniv deiakykh liniyi bdzhil pidvydu A. m. carnica [Refined morphometric standards of drone wings of some lines of bees of the subspecies A. m. carnica]. Pasika, 5, 15–16 (in Ukrainian).
Babenko, V., Galatyuk, O., Cherevatov, V., Yarovets, V., Hryhorkiv, L., Kalashnikov, O., Egoshin, L., & Romanyshyna, T. (2023). Wing morphometry of worker bees of Kharkiv, Sumy and Poltava regions of Ukraine. Animal Husbandry Products Production and Processing, 2, 78–89.
Bernstein, R., Du, M., Du, Z. G., Strauss, A. S., Hoppe, A., & Bienefeld, K. (2023). First large-scale genomic prediction in the honey bee. Heredity, 130(5), 320–328.
Bouga, M., Alaux, C., Bienkowska, M., Büchler, R., Carreck, N. L., Cauia, E., Chlebo, R., Dahle, B., Dall'Olio, R., De la Rúa, P., Gregorc, A., Ivanova, E., Kence, A., Kence, M., Kezic, N., Kiprijanovska, H., Kozmus, P., Kryger, P., Le Conte, Y., Lodesani, M., Murilhas, A. M., Siceanu, A., Soland, G., Uzunov, G., & Wilde, J. (2011). A review of methods for discrimination of honey bee populations as applied to European beekeeping. Journal of Apicultural Research, 50(1), 51–84.
Bustamante, T., Baiser, B., & Ellis, J. D. (2019). Comparing classical and geometric morphometric methods to discriminate between the South African honey bee subspecies Apis mellifera scutellata and Apis mellifera capensis (Hymenoptera: Apidae). Apidologie, 51(1), 123–136.
Calovi, M., Grozinger, C. M., Miller, D. A., & Goslee, S. C. (2021). Summer weather conditions influence winter survival of honey bees (Apis mellifera) in the northeastern United States. Scientific Reports, 11(1), 1553.
Carreira, G. P., Shaw, P. W., Gonçalves, J. M., & McKeown, N. J. (2017). Congruent molecular and morphological diversity of Macaronesian limpets: Insights into eco-evolutionary forces and tools for conservation. Frontiers in Marine Science, 4, 75.
Chauzat, M.-P., Jacques, A., Laurent, M., Bougeard, S., Hendrikx, P., & Ribière-Chabert, M. (2016). Risk indicators affecting honey bee colony survival in Europe: One year of surveillance. Apidologie, 47(3), 348–378.
Cherevatov, O. V., Melnik, E. O., & Volkov, R. A. (2020). Polimorfizm hena COI u medonosnykh bdzhil z riznykh rehioniv Ukrayiny [Polymorphism of the COI gene in honey bees from different regions of Ukraine]. Visnyk Ukrayins’koho Tovarys’tva Henetykiv i Selektsioneriv, 18(1–2), 22–28 (in Ukrainian).
Cherevatov, O. V., Panchuk, I. I., Kerek, S. S., & Volkov, R. A. (2019). Molecular diversity of the CoI-CoII spacer region in the mitochondrial genome and the origin of the Carpathian bee. Cytology and Genetics, 4, 13–14.
Donthu, R., Marcelino, J. A., Giordano, R., Tao, Y., Weber, E., Avalos, A., Band, M., Akraiko, T., Chen, S.-C., Reyes, M. P., Hao, H., Ortiz-Alvarado, Y., Cuff, C. A., Claudio, E. P., Soto-Adames, F., Smith-Pardo, A. H., Meikle, W, G., Evans, J. D., Giray, T., Abdelkader, F. B., Allsopp, M., Ball, D., Morgado, S. B., Barjadze, S., Correa-Benitez, A., Chakir, A., Báez, D. R., Chavez, N. H. M., Dalmon, A., Douglas, A. B., Fraccica, C., Fernández-Marín, H., Galindo-Cardona, A., Guzman-Novoa, E., Horsburgh, R., Meral Kence, M., Kilonzo, J., Kükrer, M., Le Conte, Y., Mazzeo, G., Mota, F., Muli, E., Oskay, D., Ruiz-Martínez, J. A., Oliveri, E., Pichkhaia, I., Romane, A., Sanchez, C. G., Sikombwa, E., Satta, A., Scannapieco, A. A., Stanford, B., Soroker, V., Velarde, R. A., Vercelli, M., & Huang, Z. (2024). HBeeID: A molecular tool that identifies honey bee subspecies from different geographic populations. BMC Bioinformatics, 25(1), 278.
Eynard, S. E., Klopp, C., Canale-Tabet, K., Marande, W., Vandecasteele, C., Roques, C., Donnadieu, C., Boone, Q., Servin, B., & Vignal, A. (2024). The black honey bee genome: Insights on specific structural elements and a first step towards pangenomes. Genetics Selection Evolution, 56(1), 51.
Faurot-Daniels, C., Glenny, W., Daughenbaugh, K. F., McMenamin, A. J., Burkle, L. A., & Flenniken, M. L. (2020). Longitudinal monitoring of honey bee colonies reveals dynamic nature of virus abundance and indicates a negative impact of Lake Sinai virus 2 on colony health. PLoS One, 15(9), e0237544.
Galatiuk, O. Y., Zastulka, M. V., Cherevatov, V. F., Yarovets, V. I., & Egoshin, L. R. (2024). Obtaining morphometric standards of drone wings of separate populations of honey bees (Apis mellifera) in Ukraine. Regulatory Mechanisms in Biosystems, 15(1), 92–96.
Geldmann, J., & Gonzalez-Varo, J. P. (2018). Conserving honey bees does not help wildlife. Science, 359(6374), 392–393.
Gilchrist, I., Nixon, J., Shultz, R., Ginzel, M., & Harpur, B. (2024). To house or oust: Honey bee (Apis mellifera) colonies can evaluate and evict drones of low quality. Behavioral Ecology and Sociobiology, 78, 47.
Gontarz, A., Banaszewska, D., Gryzinska, M., & Andraszek, K. (2016). Differences in drone sperm morphometry and activity at the beginning and end of the season. Turkish Journal of Veterinary and Animal Sciences, 40(5), 598–602.
Gray, A., Adjlane, N., Arab, A., & Ballis, A., Brusbardis, V., Douglas, A. B., Cadahía, L., Charriere, J.-D., Chiebo, R., Coffey, M. F., Cornelissen, B., da Costa, C. A., Danneels, E., Danihlik, J., Dobrescu, C., Evans, G., Fedoriak, M., Forsythe, I., Gregorc, A., Arakelyan, J. J., Johannesen, J., Kauko, L., Kristiansen, P., Martikkala, M., Martín-Hernández, R., Mazur, E., Medina-Flores, C. A., Mutinelli, F., Omar, E. O., Patalano, S., Raudmets, A., Martin, G. S., Soroker, V., Stahlmann-Brown, P., Stevanovic, J., Uzunov, A., Veisnaes, F., Anthony Williams, A., & Brodschneider, R. (2023). Honey bee colony loss rates in 37 countries using the COLOSS survey for winter 2019–2020: The combined effects of operation size, migration and queen replacement. Journal of Apicultural Research, 62(2), 204–210.
Groeneveld, L. F., Kirkerud, L. A., Dahle, B., Sunding, M., Flobakk, M., Kjos, M., Henriques, D., Pinto, M. A., & Berg, P. (2020). Conservation of the dark bee (Apis mellifera mellifera): Estimating C-lineage introgression in Nordic breeding stocks. Acta Agriculturæ Scandinavica, Section A – Animal Science, 69(1–2), 157–168.
Güler, A. (2010). A morphometric model for determining the effect of commercial queen bee usage on the native honeybee (Apis mellifera L.) population in a Turkish province. Apidologіе, 41, 622–635.
Hagan, T., Lim, J., Buchmann, G., Ding, G., Oldroyd, B. P., & Gloag, R. (2024). The use of drone congregation behaviour for population surveys of the honey bee Apis cerana. Apidologie, 55, 12.
Han, F., Wallberg, A., & Webster, M. T. (2012). From where did the Western honeybee (Apis mellifera) originate? Ecology and Evolution, 2(8), 1949–1957.
Henriques, D., Chavez-Galarza, J., Teixeira, J. S. G., Ferreira, H., Neves, C. J., Francoy, T. M., & 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), 89.
Insolia, L., Molinari, R., Rogers, S. R., Williams, G. R., Chiaromonte, F., & Calovi, M. (2022). Honey bee colony loss linked to parasites, pesticides and extreme weather across the United States. Scientific Reports, 12(1), 20787.
Jack, C. J., Boncristiani, H., Prouty, C., Schmehl, D. R., & Ellis, J. D. (2024). Evaluating the seasonal efficacy of commonly used chemical treatments on Varroa destructor (Mesostigmata: Varroidae) population resurgence in honey bee colonies. Journal of Insect Science, 24(3), 11.
Jones, J. C., Du, Z. G., Bernstein, R., Meyer, M., Hoppe, A., Schilling, E., Ableitner, M., Juling, K., Dick, R., Strauss, A. S., & Bienefeld, K. (2020) Tool for genomic selection and breeding to evolutionary adaptation: Development of a 100K single nucleotide polymorphism array for the honey bee. Ecology and Evolution, 10(13), 6246–6256.
Kekecoglu, M., Bir, S., & Kambur, M. (2023a). Determination of anatolian honeybee biodiversity by wing characters. Sociobiology, 70(3), e8333.
Kekecoglu, M., Bir, S., & Kambur, M. (2023b). New morphometric approach to discriminate honey bee (Apis mellifera L.) populations in Türkiye. Journal of Tekirdag Agricultural Faculty, 20(3), 653–662.
Klingenberg, C. (2021). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.
Koca, A. Ö., & Kandemir, İ. (2013). Comparison of two morphometric methods for discriminating honey bee (Apis mellifera L.) populations in Turkey. Turkish Journal of Zoology, 37(2), 205–210.
Krtinic, B., Francuski, L., Ludoški, J., & Milankov, V. (2016). Integrative approach revealed contrasting pattern of spatial structuring within urban and rural biotypes of Culex pipiens. Journal of Applied Entomology, 140(10), 757–774.
Leroy, T., Faux, P., Basso, B., Eynard, S., Wragg, D., & Vignal, A. (2024). Inferring long-term and short-term determinants of genetic diversity in honey bees: Beekeeping impact and conservation strategies. Molecular Biology and Evolution, 41(12), msae249.
Liu, H., Zhang, X., Huang, J., Chen, J. Q., Tian, D., Hurst, L. D., & Yang, S. (2015). Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee. Genome Biology, 16, 15.
Lorenz, C., Patané, J. S., & Suesdek, L. (2015). Morphogenetic characterisation, date of divergence, and evolutionary relationships of malaria vectors Anopheles cruzii and Anopheles homunculus. Infection, Genetics and Evolution, 35, 144–152.
Lukic, B., Raguz, N., Kovačić, M., & Curik, I., Obšteter, J., Prešern, J., Bubnič, J., Lužaić, R., Pihler, I., Mirjanić, G., Pietropaoli, M., & Puškadija, Z. (2024). Genomic diversity and population structure of Carniolan honey bee in its native habitat. BMC Genomics, 25(1), 849.
Maucourt, S., Fortin, F., Robert, C., & Giovenazzo, P. (2020). Genetic parameters of honey bee colonies traits in a Canadian selection program. Insects, 11(9), 587.
Meixner, M. D., Leta, M. A., Koeniger, N., & Fuchs, S. (2011). The honey bees of Ethiopia represent a new subspecies of Apis mellifera – Apis mellifera simensis ssp. Apidologіе, 42, 425–437.
Metlytska, O. I., Polishchu, V. P., & Vydryk, A. V. (2011). Molekuliarno-henetychni osoblyvosti bdzhil ukrayinskoyi ta karpatskoyi porid v porivnianni z oznakamy yikh eksterieru [Molecular and genetic features of bees of Ukrainian and Carpathian breeds in comparison with their exterior characteristics]. Naukovi Dopovidi Natsional’noho Universytetu Bioresursiv i Pryrodokorystuvannia Ukrayiny, 26, 4–11 (in Ukrainian).
Metz, B., & Tarpy, D. (2021). Reproductive and morphological quality of commercial honey bee (Hymenoptera: Apidae) drones in the United States. Journal of Insect Science, 21(6), 2.
Neubauer, L., Davidson, J., Wild, B., Dormagen, D., Landgraf, T., Couzin, I., & Smith, M. (2023). Honey bee drones are synchronously hyperactive inside the nest. Animal Behaviour, 203, 207–223.
Oleksa, A., Wilde, J., Tofilski, A., & Chybicki, I. J. (2013). Partial reproductive isolation between European subspecies of honey bees. Apidologie, 44, 611–619.
Özdil, F., Oskay, D., Işık, R., Yatkın, S., Aydın, A., & Güler, A. (2022). Morphometric and genetic characterization of honey bees (Apis mellifera L.) from Thrace Region of Turkiye. Journal of Apicultural Science, 66(1), 67–83.
Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., Dicks, L. V., Garibaldi, L. A., Hill, R., Settele, J., & Vanbergen, A. J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540(7632), 220–229.
Rahimi, A., Mirmoayedi, A., Kahrizi, D., Zarei, L., & Jamali, S. (2017). Morphometric diversity and phylogenetic relationships among Iranian honey bee (Apis mellifera meda Skorikow, 1829) populations using morphological characters. Sociobiology, 64(1), 33–41.
Rangel, J., & Fisher II, A. (2019). Factors affecting the reproductive health of honey bee (Apis mellifera) drones – a review. Apidologіе, 50, 759–778.
Requier, F., Antúnez, K., Morales, C. L., Sánchez, P. A., Castilhos, D., Garrido, P. M., Giacobino, A., Reynaldi, F. J., Londoño, J. M. R., Santos, E., & Garibaldi, L. A. (2018). Trends in beekeeping and honey bee colony losses in Latin America. Journal of Apicultural Research, 57(5), 657–662.
Rodrigues, P., Gomes, W., & Pinto, M. (2022). Deepwings©: Automatic wing geometric morphometrics classification of honey bee (Apis mellifera) subspecies using deep learning for detecting landmarks. Big Data and Cognitive Computing, 6, 70.
Roshka, N. M., Volkova, A. R., & Panchuk, I. I. (2021). Molecular organization of 5S ribosomal DNA of Apis mellifera ligustica. Visnik Ukrayins'kogo Tovaristva Genetikiv i Selekcioneriv, 19(1–2), 31–39.
Ruttner, F. (1988). Biogeography and taxonomy of honeybees. Springer Verlag, Berlin.
Schaumann, F., Norrström, N., Niklasson, M., & Leidenberger, S. (2024). Ecological comparison of native (Apis mellifera mellifera) and hybrid (Buckfast) honeybee drones in southwestern Sweden indicates local adaptation. PLoS One, 19(8), e0308831.
Shi, P., Zhou, J., Song, H., Wu, Y., Lan, L., Tang, X., Ma, Z., Vossbrinck, C. R., Vossbrinck, B., Zhou, Z., & Xu, J. (2020). Genomic analysis of Asian honeybee populations in China reveals evolutionary relationships and adaptation to abiotic stress. Ecology and Evolution, 10(23), 13427–13438.
Slater, G. P., Dapper, A. L., & Harpur, B. A. (2022). Haploid and sexual selection shape the rate of evolution of genes across the honey bee (Apis mellifera L.) genome. Genome Biology and Evolution, 14(6), evac063.
Sobrinho, F. C., Nunes, L. A., Silva, F. de L., & De Carvalho, C. A. L. (2023). Análise populacional do ácaro Varroa destructor (Anderson e Trueman, 2000) no nordeste do Brasil. Europub Journal of Animal and Environmental Research, 4(1), 1–23.
Tang, J., Ji, C., Shi, W., Su, S., Xue, Y., Xu, J., Chen, X., Zhao, Y., & Chen, C. (2023). Survey results of honey bee colony losses in winter in China (2009–2021). Insects, 14(6), 554.
Tatsuta, H., Takahashi, K. H., & Sakamaki, Y. (2018). Geometric morphometrics in entomology: Basics and applications. Entomological Sciennce, 21(2), 164–184.
Teichroew, J. L., Xu, J., Ahrends, A., Huang, Z., Tan, K., & Xie, Z. (2017). Is China's unparalleled and understudied bee diversity at risk? Biological Conservation, 210(B), 19–28.
Tofilski, A., Căuia, E., Siceanu, A., Vișan, G. O., & Căuia, D. (2021). Historical changes in honey beewing venation in Romania. Insects, 12, 542.
Tofilski, A., Kaur, H., & Łopuch, S. (2024). Size and shape differences in fore wings of honey bee (Apis mellifera) queens, workers and drones. Journal of Apicultural Science, 68(1), 5–17.
Utaipanon, P., Schaerf, T. M., Chapman, N. C., Holmes, M. J., & Oldroyd, B. P. (2021). Using trapped drones to assess the density of honey bee colonies: A simulation and empirical study to evaluate the accuracy of the method. Ecological Entomology, 46(1), 128–137.
Van Engelsdorp, D., & Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103(1), 80–95.
Wade, A., Lin, C-H., Kurkul, C., Regan, E. R., & Johnson, R. M. (2019). Combined toxicity of insecticides and fungicides applied to California almond orchards to honey bee larvae and adults. Insectes, 10(1), 20.
Węgrzynowicz, P., & Łoś, A. (2020). Dataset of wing venation measurements for Apis mellifera caucasica, A. mellifera carnica and A. mellifera mellifera (Hymenoptera: Apidae), their hybrids and backcrosses. Biodiversity, 8, e53724.
Williamson, E., Groom, S., Utaipanon, P., Oldroyd, B. P., Chapman, N., & Gendoorn, K. (2022). The reliability of honey bee density estimates from trapped drones. Apidologie, 53, 62.
Woodgate, J., Makinson, J., Rossi, N., Lim, Ka-Sing., Reynolds, A., Rawlings, C., & Chittka, L. (2021). Harmonic radar tracking reveals that honeybee drones navigate between multiple aerial leks. iScience, 24(6), 102499.
Yániz, J. L., Silvestre, M. A., & Santolaria, P. (2020). Sperm quality assessment in honey bee drones. Biology, 9(7), 174.
Yarovets, V. I., Cherevatov, O. V., Galatiuk, O. Y., Zastulka, M. V., & Babenko, V. V. (2024). Features of determining the subspecies status of honey bees (Apis mellifera) based on morphometric wing indicators of drones. Agrology, 7(1), 3–13.
Yevstafieva, V. O., Zaloznaya, L. M., Nazarenko, O. S., Melnychuk, V. V., & Sobolta, A. G. (2020). Morphological variation of Varroa destructor (Parasitiformes, Varroidae) in different seasons. Biosystems Diversity, 28(1), 18–23.
Zhang, L., Shao, L., Raza, M. F., Han, R., & Li, W. (2024). The effect of comb cell size on the development of Apis mellifera drones. Life, 14(2), 222.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
