Genetic Variations of the Asian Honey Bee Apis cerana Fabricius, 1793 in Kalimantan - Indonesia and Their Relationships Across Asia

Fikri Irsyad Muhammad; Rika Raffiudin; Rustem Ilyasov; Tri Atmowidi; Windra Priawandiputra; Juniarto Gautama Simanjuntak; Astuti Latif; Syafrizal Fachmi; Nova Hariani; Ahmad Muammar Kadafi; Edy Syahputra; Khaerunnisa

doi:10.13102/sociobiology.v72i4.11299

Authors

Fikri Irsyad Muhammad Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0009-0008-2275-5099
Rika Raffiudin Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0000-0002-5373-9445
Rustem Ilyasov Department of Biological Sciences, Developmental Neurobiology Laboratory, Institute of Developmental Biology of Russian Academy of Sciences, Moscow, Russia https://orcid.org/0000-0003-2445-4739
Tri Atmowidi Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0000-0002-2179-3914
Windra Priawandiputra Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0000-0002-9992-7687
Juniarto Gautama Simanjuntak Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0000-0002-8038-0466
Astuti Latif Department of Biology, Faculty of Mathematics and Natural Science, IPB University, Bogor, West Java, Indonesia https://orcid.org/0009-0008-5178-8949
Syafrizal Fachmi Department of Biology, Faculty of Mathematics and Natural Science, Mulawarman University, Samarinda, East Kalimantan, Indonesia https://orcid.org/0000-0003-1102-641X
Nova Hariani Department of Biology, Faculty of Mathematics and Natural Science, Mulawarman University, Samarinda, East Kalimantan, Indonesia https://orcid.org/0000-0001-6685-8198
Ahmad Muammar Kadafi Department of Biology, Faculty of Mathematics and Natural Science, Palangka Raya University, Palangka Raya, Central Kalimantan, Indonesia https://orcid.org/0000-0003-4646-687X
Edy Syahputra Department of Agrotechnology, Faculty of Agriculture, Tangjungpura University, Pontianak, West Kalimantan, Indonesia https://orcid.org/0000-0002-4084-3796
Khaerunnisa Department of Agribusiness, Faculty of Agriculture, Borneo Tarakan University, Tarakan, North Kalimantan, Indonesia https://orcid.org/0000-0002-8755-9311

DOI:

https://doi.org/10.13102/sociobiology.v72i4.11299

Keywords:

mitochondrial DNA, cytochrome c oxidase 1 gene, South Kalimantan, anthropogenic impact, indonesian lineage, Indo-Malayan lineage

Abstract

The vast distribution of Apis cerana (F.) across the Asian continent is a source of high genetic variations, particularly in areas experiencing geological formation and isolation, such as the Sundaland, including Kalimantan, Indonesia. This study investigated the genetic variations of A. cerana in the five provinces in Kalimantan and their relationships across Asia. We utilized mitochondrial DNA of COI, COII, and igs COI/COII sequences for genetic studies of 29 colonies from 12 locations in the five provinces of Kalimantan. The trees and network data confirmed the two lineages of A. cerana in Kalimantan, i.e., the Indo-Malayan (Borneo haplotype) and Indonesian (Java haplotype), with a slightly higher population of the latter. The high Java haplotype in Kalimantan might be due to the anthropogenic impact that transferred this honey bee from Java to Kalimantan. This finding agreed with the previous studies of geometric morphometrics using the same colonies as this study. We identified the common Borneo1 haplotype in the Indo-Malayan lineage of A. cerana, confirming previous COI findings. Furthermore, three specific haplotypes and putative amino acids of A. cerana were found in East and South Kalimantan. Those differed among the Asian population and thus could serve as the markers for these regions. Based on the sequences studied, the phylogenetic tree showed distinct clusters of A. cerana in Kalimantan and Sundaland from other A. cerana in the Asian regions. This study revealed that the mitochondrial DNA sequences showed the origin of the A. cerana population in Kalimantan and among islands in Sundaland.

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References

Anderson, D.L. (1994). Non-Reproduction of Varroa jacobsoni in Apis mellifera colonies in Papua New Guinea and Indonesia. Apidologie, 25: 412-421.

Boumans, L., Hogner, S., Brittain, J. & Johnsen, A. (2017). Ecological speciation by temporal isolation in a population of the stonefly Leuctra hippopus (Plecoptera, Leuctridae). Ecology and Evolution, 7: 1635-1649.

Boyd, O.F., Philips, T.K., Johnson, J.R. & Nixon, J.J. (2020). Geographically structured genetic diversity in the cave beetle Darlingtonea kentuckensis Valentine, 1952 (Coleoptera, Carabidae, Trechini, Trechina). Subterranean Biology, 34: 1-23.

Buchori, D., Rizali, A., Priawandiputra, W., Raffiudin, R., Sartiami, D., Pujiastuti, Y., Jauharlina, Pradana, M.G., Meilin, A., Leatemia, J.A., Sudiarta, I.P., Rustam, R., Nelly, N., Lestari, P., Syahputra, E., Hasriyanti, Watung, J.F., Daud, I.D.A., Hariani, N., Jihadi, A. & Johannis, M. (2022). Beekeeping and managed bee diversity in Indonesia: Perspective and preference of beekeepers. Diversity, 14: 52.

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 Bruyn, M., Stelbrink, B., Morley, R.J., Hall, R., Carvalho, G.R., Cannon, C.H., van den Bergh, G., Meijaard, E., Metcalfe, I., Boitani, L., Maiorano, L., Shoup, R. & von Rintelen, T. (2014). Borneo and Indochina are major evolutionary hotspots for Southeast Asian Biodiversity. Systematic Biology, 63: 879-901.

de la Rúa, P., Simon, U.E., Tilde, A.C., Moritz, R.F.A. & Fuchs, S. (2000). MtDNA variations in Apis cerana populations from the Philippines. Heredity, 84: 124-130.

Dogantzis, K.A., Raffiudin, R., Putra, R.E., Shaleh, I., Conflitti, I.M., Pepinelli, M., Roberts, J., Holmes, M., Oldroyd, B.P., Zayed, A. & Gloag, R. (2024). Post-invasion selection acts on standing genetic variation despite a severe founding bottleneck. Current Biology, 34: 1349-1356.

Engel, M. (1999). The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). Journal of Hymenoptera Research, 8: 165-196.

Estoup, A., Solignac, M., Cornuet, J.M., Goudet, J. & Scholl, A. (1996). Genetic differentiation of continental and island population of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology, 5: 19-31.

Feng, X., Huang, L., Lin, L., Yang, M. & Ma, Y. (2017). Genetic diversity and population structure of the primary malaria vector Anopheles sinensis (Diptera: Culicidae) in China inferred by cox1 gene. Parasites & Vectors, 10: 75.

Forster, M. (2020). Network 10.2.0.0. User Guide. Fluxus Technology Ltd. Retrived from: https://www.fluxus-engineering.com/Network10200_user_guide.pdf

Goodall-Copestake, W.P., Tarling, G.A. & Murphy, E.J. (2012). On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity, 109: 50-56.

Groot, A.T., Marr, M., Heckel, D.G. & Schöfl, G. (2010). The roles and interactions of reproductive isolation mechanisms in fall armyworm (Lepidoptera: Noctuidae) host strains. Ecological Entomology, 35: 105-118.

Hall, R. (2013). The palaeogeography of Sundaland and Wallacea since the Late Jurassic. Journal of Limnology, 72: 1-17.

Hebert, P.D.N., Ratnasingham, S. & de Waard, J.R. (2003). Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270: S96-S99.

Ilyasov, R.A., Park, J., Takahashi, J. & Kwon, H.K. (2018). Phylogenetic uniqueness of honeybee Apis cerana from the Korean Peninsula inferred from the mitochondrial, nuclear, and morphological data. Journal of Apicultural Science, 62: 189-214.

Ilyasov, R.A., Youn, H.G., Lee, M., Kim, K.W., Proshchalykin, M.Y., Lelej, A.S., Takahashi, J. & Kwon, H.W. (2019). Phylogenetic relationships of Russian Far-East Apis cerana with other North Asian populations. Journal of Apicultural Science, 63: 289-314.

Kahono, S., Chantawannakul, P., Engel, M.S. (2018). Social bees and the current status of beekeeping in Indonesia. In Chantawannakul, P., Williams, G., Neumann, P. (Eds.). Asian Beekeeping in the 21st Century (pp. 287-306). Springer Nature Singapore.

Konrad, A., Thompson, O., Waterston, R.H., Moerman, D.G., Keightley, P.D., Bergthorsson, U. & Katju, V. (2017). Mitochondrial mutation rate, spectrum and heteroplasmy in Caenorhabditis elegans spontaneous mutation accumulation lines of differing population size. Molecular Biology and Evolution, 34: 1319-1334.

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35: 1547-1549.

Ladoukakis, E.D. & Zouros, E. (2017). Evolution and inheritance of animal mitochondrial DNA: rules and exceptions. Journal of Biological Research-Thessaloniki, 24: 2.

Larkin, M., Blackshields, G., Brown, N.P., Chenna, R., Mcgettigan, P., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A, Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23: 2947-2948.

Latif, A., Raffiudin, R., Juliandi, B., Putra, W.P., Atmowidi, T., Muhammad, F.I., Nisa, N.R., Syahputra, E., Kadafi, A.M., Hariani, N., Fachmy, S. & Khaerunnisa. (in review). Variations of wing venation of Apis cerana in Kalimantan and related islands in Sundaland based on geometric morphometric. Journal of Insect Biodiversity.

Martin, S., Wossler, T. & Kryger, P. (2002). Usurpation of African Apis mellifera scutellata colonies by parasitic Apis mellifera capensis workers. Apidologie, 3: 215-232.

National Development Planning Agency. (2024). Indeks Pembangunan Manusia. https://simreg.bappenas.go.id/home/pemantauan/ipm. (accessed date: 19 July 2025).

Nelson, D.L. & Cox, M.M. (2005). Lehninger principles of biochemistry (4th ed.). W.H. Freeman and Company.

Okuyama, H., Tingek, S. & Takahashi, J. (2017b). The complete mitochondrial genome of the cavity-nesting honeybee, Apis cerana (Insecta: Hymenoptera: Apidae) from Borneo. Mitochondrial DNA Part B: Resources, 2: 475-476.

Okuyama, H., Wakamiya, T., Fujiwara, A., Washitani, I. & Takahashi, J. (2017a). Complete mitochondrial genome of the honeybee Apis cerana native to two remote islands in Japan. Conservation Genetics Resources, 9: 557-560.

Oleksa, A., Kusza, S. & Tofilski, A. (2021). Mitochondrial DNA suggests the introduction of honeybees of African ancestry to East-Central Europe. Insects, 12: 410.

Oleksa, A., Chybicki, I., Tofilski, A. & Burczyk, J. (2011). Nuclear and mitochondrial patterns of introgression into native dark bees (Apis mellifera mellifera) in Poland. Journal of Apicultural Research, 50: 116-129.

Pardy, J.A., Lahib, S., Noor, M.A.F. & Moehring, A.J. (2021). Intraspeciﬁc Genetic Variation for Behavioral Isolation Loci in Drosophila. Genes, 12: 11.

Purwanto, H., Soesilohadi R.C.H. & Trianto, M. (2022). Stingless bees from meliponiculture in South Kalimantan, Indonesia. Biodiversitas Journal of Biological Diversity, 23: 1254-1266.

Qiqi, W., Shaheen, T., Rong, L. & Guanghui, T. (2022). Phylogeography of walnut pest Atrijuglans hetaohei (Lepidoptera: Gelechioidea) reveals comprehensive influence of geographic barriers and human activities. Journal of Asia-Pacific Entomology, 25: 101962.

Radloff, S.E., Hepburn, C., Hepburn, H.R., Fuchs, S., Hadisoesilo, S., Tan, K., Engel, M.S. & Kuznetsov, V. (2010). Population structure and classification of Apis cerana. Apidologie, 41: 589-601.

Raﬃudin, R. & Crozier, R.H. (2007). Phylogenetic analysis of honey bee behavioural evolution. Molecular Phylogenetics and Evolution, 43: 543-552.

Raﬃudin, R. & Shullia, N.I. (2020). Phylogenies of Asian honey bees, In Ilyasov, R.A. & Kwon, H.W. (Eds.), Phylogenetics of Bees (pp. 28-57). CRC Press Taylor & Francis Group.

Raffiudin, R., Shullia, N.I., Damayanti, A.U., Wahyudi, D.T., Febiriani, T.V., Atmowidi, T., Lamerkabel, J.S.A. & Widjaja, M. C. (2022). New haplotypes of Apis cerana in Indonesia: identification from mitochondrial and major royal jelly protein 2 genes. International Journal of Tropical Insect Science, 42: 389-401.

Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003). DnaSP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics, 19: 2496-2497.

Ruttner, F. (1988). Biogeography and Taxonomy of Honeybees. Springer-Verlag.

Sayusti, T., Raffiudin, R., Atmowidi, T., Aisyah, C.N., Ludiro, F.R., Baher, R.A., Putra, R.E. & Soesilohadi, R.C.H., Purnobasuki. (2023). High genetic variations of the stingless bee Tetragonula laeviceps based on mitochondrial DNA of cytochrome c oxidase subunit 1 (co1) gene in Sumatra and Java, Indonesia. Serangga, 28: 295-311.

Schaefer, C. & Rost, B. (2012). Predict impact of single amino acid change upon protein structure. BMC Genomics, 13: S4.

Shinmura, Y., Okuyama, H., Kiyoshi, T., Lin, C., Kadowaki, T. & Takahashi, J. (2017). The complete mitochondrial genome and genetic distinction of the Taiwanese honeybee, Apis cerana (Hymenoptera: Apidae). Conservation Genetics Resources, 10: 621-626.

Simanjuntak, J.G., Priawandiputra, W., Raffiudin, R., Shullia,

N.I., Jauharlina, J., Pradana, M. G., Meilin, A., Jasmi, J., Pujiastuti, Y., Lestari, P., Ilyasov, R., Sitompul, R. & Atmowidi, T. (2024). Apis cerana Fabricius, 1793 in Sumatra: Haplotype variations of mitochondrial DNA and the molecular relationship with the Asian honey bees (Hymenoptera: Apidae). HAYATI Journal

of Biosciences, 31: 768-780.

Smith, D.R. & Hagen, R.H. (1996). The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. Journal of Kansas Entomological Society, 69: 294-310.

Smith, D.R., Villafuerte, L., Otis, G. & Palmer, M.R. (2000). Biogeography of Apis cerana F. and A. nigrocincta Smith: insights from mtDNA studies. Apidologie, 31: 265-279.

Smith, D.R., Warrit, N. & Hepburn, H.R. (2004). Apis cerana from Myanmar (Burma): unusual distribution of mitochondrial lineages. Apidologie, 35, 637-644.

Smith, D.R., Warrit, N., Otis, G.W., Thai, P.H. & Tam, D.Q. (2005). A scientific note on high variation in the non-coding mitochondrial sequences of Apis cerana from South East Asia. Journal of Apicultural Research, 44, 197-198.

Su, Y.C., Chiu, Y.F., Warrit, N., Otis, G.W. & Smith, D.R. (2023). Phylogeography and species delimitation of the Asian cavity-nesting honeybees. Insect Systematics and Diversity, 7: 1-10.

Sun, Z., Chapman, N.C., Raffiudin, R., Putra, R.E., Roberts, J., Widjaya, C., Buchmann, G., Holmes, M. & Gloag, R. (2022). Loss of mitochondrial diversity in invasive populations of Asian honey bees, Apis cerana (Hymenoptera: Apidae), in the Austral-Paciﬁc. Austral Entomology, 61, 97-103.

Takahashi, J., Wakamiya, T., Kiyoshi, T., Uchiyama, H., Yajima, S., Kimura, K. & Nomura, T. (2016). The complete mitochondrial genome of the Japanese honeybee, Apis cerana japonica (Insecta: Hymenoptera: Apidae), Mitochondrial DNA Part B: Resources, 1, 156-157.

Tan, H.W, Liu, G.H., Dong, X., Lin, R.Q., Song, H.Q., Huang, S.Y., Yuan, Z.G., Zhao, G.H. & Zhu, X.Q. (2011). The complete mitochondrial genome of the asiatic cavity-nesting honeybee Apis cerana (Hymenoptera: Apidae). PLoS ONE, 6: e23008.

Tanaka, H., Roubik, D.W., Kato, M., Liew, F. & Gunsalam, G. (2001a). Phylogenetic position of Apis nuluensis of northern Borneo and phylogeography of Apis cerana as inferred from mitochondrial DNA sequences. Insectes Sociaux, 48: 44-51.

Tanaka, H., Suka, T., Kahono, S., Samejima, H., Mohamed, M. & Roubik, D.W. (2003). Mitochondrial variation and genetic differentiation in the honey bees (Apis cerana, A. koschevnikovi, and A. dorsata) of Borneo. Tropics, 13: 107-117.

Tanaka, H., Suka, T., Roubik, D.W. & Mohamed, M. (2001b). Genetic differentiation among geographic groups of three honeybee species, Apis cerana, A. koschevnikovi, and A. dorsata, in Borneo. Nature and Human Activities, 6: 5-12.

Trianto, M. & Purwanto, H. (2020). Morphological characteristics and morphometrics of Stingless Bees (Hym.: Meliponini) in Yogyakarta, Indonesia. Biodiversitas, 21: 2619-2628.

Wang, Y.Z., Li, B.Y., Hoffmann, A.A., Cao, L.J., Gong,

Y.J., Song, W., Zhu, J.Y. & Wei, S.J. (2017). Patterns of genetic variation among geographic and host-plant associated populations of the peach fruit moth Carposina sasakii (Lepidoptera: Carposinidae). BMC Evolutionary Biology, 17: 265.

Warrit, N., Smith, D.R. & Lekprayoon, C. (2006). Genetic subpopulations of Varroa mites and their Apis cerana hosts in Thailand. Apidologie, 37: 19-30.

Willis, L.G., Winston, M.L. & Honda, B.M. (1992). Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Molecular Phylogenetics and Evolution, 1: 169-178.

Wright, S. (1978). Evolution and the Genetics of Population, Volume 4: Variability within and Among Natural Populations. University of Chicago Press.

Xu, S., Schaack, S., Seyfert, A., Choi, E., Lynch, M. & Cristescu, M.E. (2012). High mutation rates in the mitochondrial genomes of Daphnia pulex. Molecular Biology and Evolution, 29: 763-769.

Zhao, W., Tan, K., Zhou, D., Wang, M., Cheng, C., Yu, Z., Miao, Y. & He, S. (2014). Phylogeographic analysis of Apis cerana populations on Hainan Island and southern mainland China, based on mitochondrial DNA sequences. Apidologie, 45: 21-33.

Zhu, X., Zhou, S., Xu, X., Wang, J., Yu, Y., Yang, K. C., Luo, Q., Xu, Y., Wang, S. & Zhou, B. (2017). Morphological differentiation in Asian honey bee (Apis cerana) populations in the basin and highlands of southwestern China. Journal of Apicultural Research, 56: 203-209.