The molecular phylogenetic signature of Bali cattle revealed by maternal and paternal markers

Molecular Biology Reports volume 40, pages5165–5176(2013)Cite this article

Abstract

Bali cattle is a domestic cattle breed that can be found in Malaysia. It is a domestic cattle that was purely derived from a domestication event in Banteng (Bos javanicus) around 3,500 BC in Indonesia. This research was conducted to portray the phylogenetic relationships of the Bali cattle with other cattle species in Malaysia based on maternal and paternal lineage. We analyzed the cytochrome c oxidase I (COI) mitochondrial gene and SRY of Y chromosome obtained from five species of the Bos genus (B. javanicus, Bos gaurus, Bos indicus, Bos taurus, and Bos grunniens). The water buffalo (Bubalus bubalis) was used as an outgroup. The phylogenetic relationships were observed by employing several algorithms: Neighbor-Joining (PAUP version 4.0), Maximum parsimony (PAUP version 4.0) and Bayesian inference (MrBayes 3.1). Results from the maternal data showed that the Bali cattle formed a monophyletic clade, and together with the B. gaurus clade formed a wild cattle clade. Results were supported by high bootstrap and posterior probability values together with genetic distance data. For the paternal lineage, the sequence variation is low (with parsimony informative characters: 2/660) resulting an unresolved Neighbor-Joining tree. However, Bali cattle and other domestic cattle appear in two monophyletic clades distinct from yak, gaur and selembu. This study expresses the potential of the COI gene in portraying the phylogenetic relationships between several Bos species which is important for conservation efforts especially in decision making since cattle is highly bred and hybrid breeds are often formed. Genetic conservation for this high quality beef cattle breed is important by maintaining its genetic characters to prevent extinction or even decreased the genetic quality.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Wilson DE, Reeder DAM (2005) Mammal species of the world: a taxonomic and geographic reference third edition. Johns Hopkins University Press, Baltimore

    Google Scholar 

  2. 2.

    Porter V (2008) The field guide to cattle, 1st edn. Voyageur Press, St Paul USA

    Google Scholar 

  3. 3.

    Loftus RT, Machugh DE, Bradley DG et al (1994) Evidence for two independent domestications of cattle. Evolution 91:2757–2761

    CAS  Google Scholar 

  4. 4.

    Yu Y, Nie L, He Z et al. (1999). Mitochondrial DNA variation in cattle of south China: origin and introgression. Analysis (January): 245–250

  5. 5.

    Rosli MK, Zakaria SS, Syed-Shabthar SMF et al (2011) Phylogenetic relationships of Malayan gaur with other species of the genus Bos based on cytochrome b gene DNA sequences. Genet Mol Res 10(1):482–493

    PubMed  Article  CAS  Google Scholar 

  6. 6.

    Cai X, Chen H, Lei CZ et al (2007) MtDNA diversity and genetic lineages of eighteen cattle breeds from Bos taurus and Bos indicus in China. Genetica 131:175–183

    PubMed  Article  Google Scholar 

  7. 7.

    MacEachern S, Mc-Ewan J, Goddard M (2009) Phylogenetic reconstruction and the identification of ancient polymorphism in the Bovini tribe (Bovidae, Bovinae). BMC Genomics 10:177

    PubMed  Article  Google Scholar 

  8. 8.

    Bradley DG, MacHugh DE, Cunningham P et al (1996) Mitochondrial diversity and the origin of African and European cattle. Proc Natl Acad Sci USA 93:5131–5135

    PubMed  Article  CAS  Google Scholar 

  9. 9.

    Mohamad K, Olsson M, Van-Tol HTA et al (2009) On the origin of Indonesian cattle. PLoS One 4(5):e5490

    PubMed  Article  Google Scholar 

  10. 10.

    Mohamad K, Olsson M, Andersson G et al (2012) The origin of Indonesian cattle and consernation genetics of thhe Bali cattle breed. Reprod Domest Anim 47:18–20

    PubMed  Article  Google Scholar 

  11. 11.

    Whitten T, Soeriaatmadja RE, Afiff SA (2006) The Ecology of Java and Bali, vol II. Periplus Editions (HK) Limited, Singapore

    Google Scholar 

  12. 12.

    Kikkawa Y, Amano T, Suzuki H (1995) Analysis of genetic diversity of domestic cattle in east and Southeast Asia in terms of variations in restriction sites and sequences of mitochondrial DNA. Biochem Genet 33:51–60

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Talib C, Entwistle K, Siregar A et al (2003) Survey of population and production dynamics of Bali cattle and existing breeding programs in Indonesia. In: Entwistle K, Lindsay D (eds.) Proceeding of strategies to improve Bali cattle in Eastern Indonesia, Brisbane: ACIAR

  14. 14.

    Noor RR, Farajallaip A, Karmitai M (2001) Pengujian kemurnian sapi Bali dengan analisis hemoglobin dengan metode lsoelectric focusing. Hayati 8(4):107–111

    Google Scholar 

  15. 15.

    Ang KC, Leow JWH, Ng BH et al (2011) Phylogenetic relationships of the Orang Asli and Iban of Malaysia based on maternal markers. Genet Mol Res 10:640–649

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Tobe SS, Kitchener AC, Linacre AMT (2010) Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome b and cytochrome oxidase subunit I mitochondrial genes. PLoS One 5(11):e14156

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Md-Zain BM, Lee SJ, Lakim M et al (2010) Phylogenetic position of Tarsius bancanus based on partial cytochrome b DNA sequences. J Biol Sci 10:348–354

    Article  CAS  Google Scholar 

  18. 18.

    Vun VF, Mahani MC, Lakim M et al (2010) Phylogenetic relationships of leaf monkeys (Presbytis; Colobinae) based on cytochrome b and 12S rRNA genes. Genet Mol Res 10:368–381

    Article  Google Scholar 

  19. 19.

    Md-Zain BM, Mohamad M, Ernie-Muneerah MA et al (2010) Phylogenetic relationships of Malaysian monkeys, Cercopithecidae, based on mitochondrial cytochrome c sequences. Genet Mol Res 9(4):1987–1996

    PubMed  Article  CAS  Google Scholar 

  20. 20.

    Parma P, Maria F, Greppi G, Enne G (2004) The complete coding region sequence of river buffalo (Bubalus bubalis) SRY gene. DNA Seq 15(1):77–80

    PubMed  CAS  Google Scholar 

  21. 21.

    Nijman IJ, Otsen M, Verkaar EL et al (2003) Hybridization of banteng (Bos javanicus) and zebu (Bos indicus) revealed by mitochondrial DNA, satellite DNA, AFLP and microsatellites. Heredity 90(1):10–16

    Article  CAS  Google Scholar 

  22. 22.

    Kirby GWM (1979) Bali cattle in Australia. World Anim Rev 31:24–29

    Google Scholar 

  23. 23.

    Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond 270:313–321

    Article  CAS  Google Scholar 

  24. 24.

    Sruoga V, Stunžėnas V, Paulavičiūtė B (2009) COI Gene as a molecular marker of Elachista Species (Lepidoptera: Elachistidae: Elachistinae) from different lithuanian populations. Proc Latv Acad Sci Sect B Nat Exact Appl Sci 63(1):21–24

    Google Scholar 

  25. 25.

    Weibel AC, Moore WS (2002) Molecular phylogeny of a cosmopolitan group of woodpeckers (genus Picoides) based on COI and Cyt b mitochondrial gene sequences. Mol Phylognet Evol 22(1):65–75

    Article  CAS  Google Scholar 

  26. 26.

    Wu YH, Xia L, Zhang Q et al (2010) Genetic diversity in the male-specific SRY gene of Lepus yarkandensis. Chin Sci Bull 55:834–840

    Article  CAS  Google Scholar 

  27. 27.

    Nijman IJ, Dick CJ, Bixtel V et al (2008) Phylogeny of Y chromosomes from bovine species. Cladistics 24:723–726

    Article  Google Scholar 

  28. 28.

    Jia S, Zhou Y, Lei C et al (2010) A new insight into cattle’s maternal origin in six Asian countries. J Genet Genom 37(3):173–180

    Article  CAS  Google Scholar 

  29. 29.

    Gudewar J, Pan D, Bera AK et al (2009) Molecular characterization of Echinococcus granulosus of Indian animal isolates on the basis of nuclear and mitochondrial genotype. J Clin Pathol 36:1381–1385

    CAS  Google Scholar 

  30. 30.

    Zainudin R, Shukor MN, Ahmad N et al (2010) Genetic structure of Hylarana erythraea (Amphibia: Anura: Ranidae) from Malaysia. Zool Stud 49(5):688–702

    CAS  Google Scholar 

  31. 31.

    Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Huelsenbeck JP, Ronquist R (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    PubMed  Article  CAS  Google Scholar 

  33. 33.

    Leache AD, Reeder TW (2002) Molecular systematics of the eastern fence lizard (Sceloporus undulatus): a comparison of parsimony, likelihood, and Bayesian approaches. Syst Biol 51:44–68

    PubMed  Article  Google Scholar 

  34. 34.

    Swofford DL (2002) Phylogenetic analysis using parsimony and other methods version 4.0 beta version. Sunderland: Sinauer Associates

  35. 35.

    Brown WM (1985) The mitochondrial genome of animals. In: Maclntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 95–130

    Google Scholar 

  36. 36.

    Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  37. 37.

    Kandil OM, Mahmoud MS, Allam NA, Namaky AH (2010) Mitochondrial cytochrome c oxidase subunit 1 (cox 1) gene sequence of the Hymenolepis species. J Am Sci 6(12):640–647

    Google Scholar 

  38. 38.

    Hassanin A, Ropiquet A (2004) Molecular phylogeny of the tribe Bovini (Bovidae, Bovinae) and the taxanomic status of the Kouprey, Bos sauveli Urbain 1937. Mol Phylogenet Evol 33:896–907

    Article  CAS  Google Scholar 

  39. 39.

    Verkaar ELC, Nijman IJ, Beeke M et al (2004) Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Mol Biol Evol 21(7):1165–1170

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Hassanin A, Ropiquet A, Cornette R et al (2006) Has the kourpey (Bos sauveli Ubain, 1937) been domesticated in Cambodia? C R Biol 329:124–135

    PubMed  Article  Google Scholar 

  41. 41.

    Ma G, Chang H, Li S et al (2007) Phylogenetic relationships and status quo of colonies for gayal based on analysis of cytochrome b gene partial sequences. J Genet Genomics 34(5):413–419

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Beja-pereira A, Caramelli D, Lalueza-fox C et al (2006) The origin of European cattle: evidence from modern and ancient DNA. Proc Natl Acad Sci USA 103(21):8113–8118

    PubMed  Article  CAS  Google Scholar 

  43. 43.

    Kikkawa Y, Takada T, Nomura K et al (2003) Phylogenies using mtDNA and SRY provide evidence for male-mediated introgression in Asian domestic cattle. Society 34:96–101

    CAS  Google Scholar 

  44. 44.

    Stock F, Edwards CJ, Bollongino R et al (2009) Cytochrome b sequences of ancient cattle and wild ox support phylogenetic complexity in the ancient and modern bovine population. Anim Genet 40:694–700

    PubMed  Article  CAS  Google Scholar 

  45. 45.

    Troy CS, Machugh DE, Bailey JF (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature 410(April):1088–1092

    PubMed  Article  CAS  Google Scholar 

  46. 46.

    Hassanin A, Ropiquet A (2007) What is the taxonomic status of the Cambodian banteng and does it have close genetic links with the kouprey? J Zool 27(3):246–252

    Article  Google Scholar 

  47. 47.

    Li ZC, Xia L, Li YM et al (2006) Mitochondrial DNA variation and population structure of the yarkand hare Lepus yarkandensis. Acta Theriol 51:243–253

    Article  Google Scholar 

  48. 48.

    Abdullah MH, Idris I, Hilmi M (2009) Karyotype of Malayan gaur (Bos gaurus hubbacki), shahiwal-fresian cattle and gaur x cattle hybrid backcrosses. Pak J Biol Sci 12(12):896–901

    Article  Google Scholar 

  49. 49.

    Hellborg L, Ellegren H (2004) Low levels of nucleotide diversity in mammalian Y chromosomes. Mol Biol Evol 21:158–163

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    Brandli L, Handley LJ, Vogel P, Perrin N (2005) Evolutionary history of the greater white-toothed shrew (Crocidura russula) inferred from analysis of mtDNA, Y, and X chromosome markers. Mol Phylogenet Evol 37:832–844

    PubMed  Article  Google Scholar 

  51. 51.

    Lawson LJ, Hewitt GM (2002) Comparison of substitution rates in ZFX and ZFY introns of sheep and goat related species supports the hypothesis of male-biased mutation rates. J Mol Evol 54:54–61

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Hughes JF, Skaletsky H, Pyntikova T et al (2005) Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee. Nature 437:100–103

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We would like to express our sincere appreciation to the Faculty of Science and Technology, UKM. We also thank the Agro-Biotechnology Institute (ABI), MOSTI. Our special thanks to the Department of Wildlife and National Parks (PERHILITAN), especially the Director General, Director Ex-situ Conservation Division (Saharudin Anan) and Jeffrine Rovie Ryan Japning and the National Institute of Veterinary Biodiversity (IBVK) for providing genetic samples. This study was funded by research grants STGL-003-2009 and 08-05-ABI-AB032/1 received from the Agro-Biotechnology Institute (ABI), MOSTI, Sciencefund 02-01-02-SF0762, INDUSTRI-2011-003, DLP-2013-006 and UKM-OUP-2012-043. We also express our gratitude to all who were directly or indirectly involved in this study.

Author information

Affiliations

  1. School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600, Bangi, Selangor, Malaysia

    S. M. F. Syed-Shabthar, M. K. A. Rosli, N. A. A. Mohd-Zin, M. C. Mahani, S. Yaakop & B. M. Md-Zain

  2. Agro-Biotechnology Institute, Malaysia (ABI), 43400, Serdang, Selangor, Malaysia

    S. M. N. Romaino, Z. A. Fazly-Ann & O. Abas-Mazni

  3. Molecular Ecology Laboratory, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia

    R. Zainuddin

Authors
  1. S. M. F. Syed-Shabthar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. K. A. Rosli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. A. A. Mohd-Zin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. M. N. Romaino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Z. A. Fazly-Ann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. C. Mahani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. O. Abas-Mazni
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Zainuddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. Yaakop
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. B. M. Md-Zain
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. M. Md-Zain.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Syed-Shabthar, S.M.F., Rosli, M.K.A., Mohd-Zin, N.A.A. et al. The molecular phylogenetic signature of Bali cattle revealed by maternal and paternal markers. Mol Biol Rep 40, 5165–5176 (2013). https://doi.org/10.1007/s11033-013-2619-y

Download citation

Keywords

  • Bali cattle
  • Bos javanicus
  • Gaur
  • Cytochrome
  • C oxidase I
  • SRY gene