Haplotype Diversity of Swamp Buffalo and River Buffalo Based on Cytochrome B Gene: A Study of Meta-Analysis

  • F. Saputra Indonesian Research Institute for Animal Production http://orcid.org/0000-0002-7949-9777
  • A. Anggraeni Indonesian Research Institute for Animal Production
  • A. B. L. Ishak Indonesian Research Institute for Animal Production
  • A. Hafid Indonesian Research Institute for Animal Production
  • M. Rusdin Department of Animal Science, Faculty of Animal Science, Halu Oleo University
  • C. Sumantri Department of Animal Production and Technology, Faculty of Animal Science, IPB University
Keywords: haplotype diversity, swamp buffalo, cytochrome b, meta-analysis


Buffalo (Bubalus bubalis) is well known as a domesticated buffalo in Asia. The genetic diversity of buffaloes in Asia needs to be studied to ensure a proper breeding program. A meta-analysis study on the cytochrome b gene of the mitochondrial genome from various published data was conducted to evaluate genetic variation and haplo-geography of Asian buffaloes. A meta-analysis is used to provide a comprehensive view of the data. A total of 1369 swamp buffaloes Cytochrome B sequences (from Indonesia (79), Bangladesh (98), China (909), India (4), Laos (96), Taiwan (29), Thailand (54), and Vietnam (100)) and 91 river buffaloes (from China (42), Nepal (42), and Pakistan (7)) were used in this study. Cytochrome B sequences (678 bp) of Syncerus caffer, Bubalus arnee, Bubalus depressicornis, Bubalus quarlesi, Bubalus mindorensis, swamp buffalo, and river buffalo were determined for their haplotypes using DnaSP v6 program. Haplotypes were analyzed by Principal Coordinate Analysis (PCoA) using Adegenet Package and Hierarchical Clustering on Principal Components (HCPC) methods using Factoextra and FactoMineR Package in R-4.0.0 program. Bayesian analysis of genetic differentiation was implemented in BAPS 6.0. Furthermore, we found 56 haplotypes for swamp buffaloes in eight Asian countries and 5 haplotypes for river buffaloes in Pakistan. We also found 5 haplotypes for outgroup (B. arnee, S. caffer, B. depressicornis, B. quarlesi, B. mindorensis). Therefore, we found 66 haplotypes in total with outgroup sequences. Based on the PCoA results, three clusters were found. However, the HCPC found eight clusters. Based on HCPC, countries in East and South Asia have four maternal lineages. This is evidence that buffalo domestication has first occurred in East-South Asia. In conclusion, we found four maternal lineages of swamp buffalo and two maternal lineages of river buffalo from ten countries. We also found one maternal lineage for Syncerus caffer and one maternal lineage for B. depressicornis, B. quarlesi, and B. mindorensis.


Download data is not yet available.


Andreas, E., C. Sumantri, H. Nuraini, A. Farajallah, & A. Anggraeni. 2010. Identification of GH|ALUI and GHR|ALUI genes polymorphisms in Indonesian Buffalo. J. Indonesian Trop. Anim. Agric. 35:215–221. https://doi.org/10.14710/jitaa.35.4.215-221

Cheng, L., T. R. Connor, J. Sirén, D. M. Aanensen, & J. Corander. 2013. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol. Biol. Evol. 30:1224–1228. https://doi.org/10.1093/molbev/mst028

Chikuni, K., Y. Mori, T. Tabata, M. Saito, M. Monma, & M. Kosugiyama. 1995. Molecular phylogeny based on the κ-casein and cytochrome b sequences in the mammalian suborder Ruminantia. J. Mol. Evol. 41:859–866. https://doi.org/10.1007/BF00173165

Guangxin, E., Z. Yong-Ju, N. Ri-Su, M. Yue-Hui, Z. Jia-Hua, C. LiPeng, Q. Xiao-Yu, Z. Zhong-Quan, S. Ya-Wang, W. Xin, & H. Yong-Fu. 2016. Meta-analysis evidence of maternal lineages in Chinese Tibetan sheep using mtDNA D-loop panel, Mitochondrial DNA Part A. https://doi.org/10.3109/24701394.2016.1143469

Husson, F., J. Josse, S. Le, & J. Mazet. 2015. FactoMineR: Multivariate Exploratory Data Analysis and Data Mining. R Package Version 1.31.4. 24:1–18.

Jombart, T. 2008. Adegenet: A R package for the multivariate analysis of genetic markers. Bioinform. 11:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

Kassambara, A., & F. Mundt. 2020. factoextra: Extract and Visualize the Results of Multivariate Data Analyses (R package version 1.0.7). https://cran.r-project.org/package=factoextra

Kumar, S., M. Nagarajan, J. S. Sandhu, N. Kumar, V. Behl, & G. Nishanth. 2007. Mitochondrial DNA analyses of Indian water buffalo support a distinct genetic origin of river and swamp buffalo. Anim. Genet. 38:227–232. https://doi.org/10.1111/j.1365-2052.2007.01602.x

Kumar, S., G. Stecher, & K. Tamura. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33:1870–1874. https://doi.org/10.1093/molbev/msw054

Lei, C. Z., C. M. Zhang, S. Weining, M. G. Campana, M. A. Bower, X. M. Zhang, L. Liu, X. Y. Lan, & H. Chen. 2011. Genetic diversity of mitochondrial cytochrome b gene in Chinese native buffalo. Anim. Genet. 42:432–436. https://doi.org/10.1111/j.1365-2052.2011.02174.x

Lei, C. Z., W. Zhang, H. Chen, F. Lu, Q. L. Ge, R. Y. Liu, R. H. Dang, Y. Y. Yao, L. B. Yao, Z. F. Lu, & Z. L. Zhao. 2007. Two maternal lineages revealed by mitochondrial DMA D-loop sequences in Chinese native water buffaloes (bubalus bubalis). Asian-Australas. J. Anim. Sci. 20:471–476. https://doi.org/10.5713/ajas.2007.471

Luo, X., Y. Zhou, B. Zhang, Y. Zhang, X. Wang, T. Feng, Z. Li, K. Cui, Z. Wang, C. Luo, H. Li , Y. Deng, F. Lu , J. Han, Y. Miao, H. Mao, X. Yi , C. Ai, S. Wu, A. Li, Z. Wu, Z. Zhuo, D. D. Giang, B. Mitra, M. F. Vahidi, S. Mansoor, S. Ahmed Al-Bayatti, Eka Meutia Sari, N. A. Gorkhali, S. Prastowo, L. Shafique, G. Ye, Q. Qian, B. Chen, D. Shi, J. Ruan, & Q. Liu. 2020. Understanding divergent domestication traits from the whole-genome sequencing of swamp-and river-buffalo populations. Natl. Sci. Rev. 7:686–701. https://doi.org/10.1093/nsr/nwaa024

Mastrochirico-Filho, V. A., F. Pazo. M. E. Del Hata, G. V. Villanova, F. Foresti, M. Vera, P. Martínez, F. Porto-Foresti, & D. T. Hashimoto. 2019. Assessing genetic diversity for a pre-breeding program in piaractus mesopotamicus by snps and ssrs. Genes. 10:668. https://doi.org/10.3390/genes10090668

Misrianti, R., C. Sumantri, & A. Farajallah. 2010. Polymorphism identification of pit1 gene in indonesian buffaloes (Bubalus bubalis) and holstein-friesian cows. Media Peternakan. 33:131–136. https://doi.org/10.5398/medpet.2010.33.3.131

Nagarajan, M., K. Nimisha, & S. Kumar. 2015. Mitochondrial DNA variability of domestic River buffalo (Bubalus bubalis) populations: Genetic evidence for domestication of River buffalo in Indian subcontinent. Genome. Biol. Evol. 7:1252–1259. https://doi.org/10.1093/gbe/evv067

Paraguas, A. M., T. P. C. Cailipan, E. B. Flores, & L. P. Villamor. 2018. Morphology and phylogeny of swamp buffaloes (Bubalus bubalis) in Calayan Island, Cagayan. Philipp. J. Vet. Anim. Sci. 44:59-67.

R Core, T. 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.r-project.org/

Rozas, J., A. Ferrer-Mata, J. C. Sanchez-Del Barrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins, & A. Sanchez-Gracia. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34:3299–3302. https://doi.org/10.1093/molbev/msx248

Rusdin, M., D. D. Solihin, A. Gunawan, C. Talib, & C. Sumantri. 2020. Genetic variation of eight Indonesian swamp-buffalo populations based on cytochrome b gene marker. Trop. Anim. Sci. J. 3:1–10. https://doi.org/10.5398/tasj.2020.43.1.1

Saif, R., M. Wasim, & M. E. Babar. 2012. Molecular phylogeny of Pakistani riverine buffalo based on genetic variability of Mitochondrial cytochrome b gene. Mol. Biol. Rep. 39:9707–9714. https://doi.org/10.1007/s11033-012-1835-1

Saputra, F., Jakaria, A. Anggraeni, & C. Sumantri. 2020. Genetic diversity of Indonesian swamp buffalo based on microsatellite markers. Trop. Anim. Sci. J. 43:191–196. https://doi.org/10.5398/tasj.2020.43.3.191

Saputra, F., Jakaria, & C. Sumantri. 2013. Genetic variation of mtDNA cytochrome oxidase subunit I (COI) in Local swamp buffaloes in Indonesia. Med. Pet. 36:165–170. https://doi.org/10.5398/medpet.2013.36.3.165

Sumantri, C., R. Diyono, A. Farajallah, A. Anggraeni, & E. Andreas. 2010. Pemanfaatan famili gen hormon pertumbuhan (GH, GHR, GHRH, dan PIT-1) untuk mendeteksi keragaman genetik kerbau di Kabupaten Pandeglang dan Lebak Provinsi Banten. Jurnal Ilmu Ternak dan Veteriner 15:286–296.

Sun, T., S. Wang, Q. Hanif, N. Chen, H. Chen, & C. Lei. 2020. Genetic diversity of mitochondrial cytochrome b gene in swamp buffalo. Anim. Genet. 51:977-981. https://doi.org/10.1111/age.12997

Taberlet, P., E. Coissac, J. Pansu, & F. Pompanon. 2011 Conservation genetics of cattle, sheep, and goats. C. S. Biologies. 334:247-254. https://doi.org/10.1016/j.crvi.2010.12.007

Tanaka, K., C. D. Solis, J. S. Masangkay, K. I. Maeda, Y. Kawamoto, & T. Namikawa. 1996. Phylogenetic relationship among all living species of the genus Bubalus based on DNA sequences of the cytochrome b gene. Biochem. Genet. 34:443–452. https://doi.org/10.1007/BF00570125

Tobe, S. S., A. C. Kitchener, & A. M. T. Linacre. 2010. Reconstructing mammalian phylogenies: A detailed comparison of the cytochrome b and cytochrome oxidase subunit i mitochondrial genes. PLoS ONE. 5:e14156. https://doi.org/10.1371/journal.pone.0014156

Wang, S., N. Chen, M. R. Capodiferro, T. Zhang, H. Lancioni, H. Zhang, Y. Miao, V. Chanthakhoun, M. Wanapat, M. Yindee, Y. Zhang, H. Lu, L. Caporali, R. Dang, Y. Huang, X. Lan, M. Plath, H. Chen, J. A. Lenstra, A. Achilli & C. Lei. 2017. Whole mitogenomes reveal the history of swamp buffalo: initially shaped by glacial periods and eventually modelled by domestication. Sci Rep 7:4708 (2017). https://doi.org/10.1038/s41598-017-048

Youssef, N. A., M. Curaudeau, S. M. El Nahas, A. A. M. Hassan & A. Hassanin. 2021. Haplotype diversity in the mitochondrial genome of the Egyptian river buffalo (Bubalus bubalis). Mitochondrial DNA B Resour. 6:145-147. https://doi.org/10.1080/23802359.2020.1852622

Zhang, Yi, Y. Lu, M. Yindee, K-Y. Li, H-Y. Kuo, Y-T. Ju, S. Ye, M. O. Faruque, Q. Li, Y. Wang, V. C. Cuong, L. D. Pham, B. Bouahom, B. Yang, X. Liang, Z. Cai, D. Vankan, W. Manatchaiworakul, N. Kowlim, S. Duangchantrasiri, W. Wajjwalku, B. Colenbrander, Y. Zhang, P. Beerli, J. A. Lenstra, & J. F. S. Barker. 2016. Strong and stable geographic differentiation of swamp buffalo maternal and paternal lineages indicates domestication in the China/Indochina border region. Mol. Ecol. 25:1530–1550. https://doi.org/10.1111/mec.13518

Zhang, Y., L. Colli, & J. S. F. Barker. 2020. Asian water buffalo: domestication, history and genetics. Anim. Genet. 51:177–191. https://doi.org/10.1111/age.12911

How to Cite
SaputraF., AnggraeniA., IshakA. B. L., HafidA., RusdinM., & SumantriC. (2021). Haplotype Diversity of Swamp Buffalo and River Buffalo Based on Cytochrome B Gene: A Study of Meta-Analysis. Tropical Animal Science Journal, 44(4), 399-407. https://doi.org/10.5398/tasj.2021.44.4.399