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  • 1 Kaposvár University, Guba Sándor u. 40, H-7400 Kaposvár, Hungary
  • 2 Agricultural Biotechnology Institute — National Agricultural Research and Innovation Center, Szent-Györgyi Albert u. 4, H-2100 Gödöllő, Hungary
  • 3 Game Management Landscape Center of Kaposvár University, Malom u. 3, H-7475 Bőszénfa, Hungary
  • 4 Eötvös Loránd University, Pázmány Péter s. 1/c, H-1117 Budapest, Hungary
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Recently, there has been considerable interest in genetic differentiation in the Cervidae family. A common tool used to determine genetic variation in different species, breeds and populations is mitochondrial DNA analysis, which can be used to estimate phylogenetic relationships among animal taxa and for molecular phylogenetic evolution analysis. With the development of sequencing technology, more and more mitochondrial sequences have been made available in public databases, including whole mitochondrial DNA sequences. These data have been used for phylogenetic analysis of animal species, and for studies of evolutionary processes.

We determined the complete mitochondrial genome of a Central European red deer, Cervus elaphus hippelaphus, from Hungary by a next generation sequencing technology. The mitochondrial genome is 16 354 bp in length and contains 13 protein-coding genes, two rRNA genes, 22 tRNA genes and a control region, all of which are arranged similar as in other vertebrates. We made phylogenetic analyses with the new sequence and 76 available mitochondrial sequences of Cervidae, using Bos taurus mitochondrial sequence as outgroup. We used ‘neighbor joining’ and ‘maximum likelihood’ methods on whole mitochondrial genome sequences; the consensus phylogenetic trees supported monophyly of the family Cervidae; it was divided into two subfamilies, Cervinae and Capreolinae, and five tribes, Cervini, Muntiacini, Alceini, Odocoileini, and Capreolini. The evolutionary structure of the family Cervidae can be reconstructed by phylogenetic analysis based on whole mitochondrial genomes; which method could be used broadly in phylogenetic evolutionary analysis of animal taxa.

  • 1.

    Bán, I. (1998) The Hungarian Wonder Deer. EP Systema, Debrecen.

  • 2.

    Douzery, E., Randi, E. (1997) The mitochondrial control region of Cervidae: Evolutionary patterns and phylogenetic content. Mol. Biol. Evol. 14, 11541166.

    • Search Google Scholar
    • Export Citation
  • 3.

    Feulner, P. G. D., Bielfeldt, W., Zachos, F. E., Bradvarovic, J., Eckert, I., Hartl, G. B. (2004) Mitochondrial DNA and microsatellite analyses of the genetic status of the presumed subspecies Cervus elaphus montanus (Carpathian red deer). Heredity 93, 299306.

    • Search Google Scholar
    • Export Citation
  • 4.

    Flegontov, P., Gray, M. W., Burger, G., Lukes, J. (2011) Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr. Genet. 57, 225232.

    • Search Google Scholar
    • Export Citation
  • 5.

    Gilbert, C., Ropiquet, A., Hassanin, A. (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia). Systematics, morphology, and biogeography. Mol. Phylogenet. Evol. 40, 101117.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hahn, C., Bachmann, L., Chevreux, B. (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads –a baiting and iterative mapping approach. Nucl. Acids Res. 41, e129.

    • Search Google Scholar
    • Export Citation
  • 7.

    Hassanin, A., Delsuc, F., Ropiquet, A., Hammer, C., Jansen van Vuuren, B., Matthee, C., Ruiz-Garcia, M., Catzeflis, F., Areskoug, V., Nguyen, T. T., Couloux, A. (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C. R. Biol. 335, 3250.

    • Search Google Scholar
    • Export Citation
  • 8.

    Ju, Y., Liu, H., Rong, M., Yang, Y., Wei, H., Shao, Y., Chen, X., Xing, X. (2016) Complete mitochondrial genome sequence of Aoluguya reindeer (Rangifer tarandus). Mitochondrial DNA 27, 22612262.

    • Search Google Scholar
    • Export Citation
  • 9.

    Kuwayama, R., Ozawa, T. (2000) Phylogenetic relationships among European red deer, wapiti, and sika deer inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 15, 115123.

    • Search Google Scholar
    • Export Citation
  • 10.

    Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., 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, 29472948.

    • Search Google Scholar
    • Export Citation
  • 11.

    Lartillot, N., Lepage, T., Blanquart, S. (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 22862288.

    • Search Google Scholar
    • Export Citation
  • 12.

    Li, Y., Ba, H., Yang, F. (2016) Complete mitochondrial genome of Cervus elaphus songaricus (Cetartiodactyla: Cervinae) and a phylogenetic analysis with related species. Mitochondrial DNA 620621.

    • Search Google Scholar
    • Export Citation
  • 13.

    Liu, Z., Wang, J., Sun, Y., Hou, Z., Teng, L. (2015) Complete mitochondrial genome of a wild Alashan Red Deer (Cervus elaphus alxaicus). Mitochondrial DNA Early Online.

    • Search Google Scholar
    • Export Citation
  • 14.

    Lowe, T. M., Eddy, S. R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl. Acids Res. 25, 955964.

    • Search Google Scholar
    • Export Citation
  • 15.

    Mahmut, H., Masuda, R., Onuma, M., Takahashi, M., Nagata, J., Suzuki, M., Ohtaishi, N. (2002) Molecular phylogeography of the red deer (Cervus elaphus) populations in Xinjiang of China: Comparison with other Asian, European, and North American populations. Zool. Sci. 19, 485495.

    • Search Google Scholar
    • Export Citation
  • 16.

    Marincs, F., Molnár, J., Tóth, G., Stéger, V., Barta, E. (2013) Introgression and isolation contributed to the development of Hungarian Mangalica pigs from a particular European ancient bloodline. Genet. Sel. Evol. 45, 22.

    • Search Google Scholar
    • Export Citation
  • 17.

    Matosiuk, M., Sheremetyeva, I. N., Sheremetyev, I. S., Saveljev, A. P., Borkowska, A. (2014) Evolutionary neutrality of mtDNA introgression: evidence from complete mitogenome analysis in roe deer. J. Evol. Biol. 27, 24832494.

    • Search Google Scholar
    • Export Citation
  • 18.

    Milner, J. M., Bonenfant, C., Mysterud, A., Gaillard, J. M., Csányi, S., Stenseth, N. C. (2006) Temporal and spatial development of red deer harvesting in Europe: biological and cultural factors. J. Appl. Ecol. 43, 721734.

    • Search Google Scholar
    • Export Citation
  • 19.

    Molnár, J., Tóth, G., Stéger, V., Zsolnai, A., Jánosi, A., Mohr, A., Szántó-Egész, R., Tóth, P., Micsinai, A., Rátky, J., Marincs, F. (2013) Mitochondrial D-loop analysis reveals low diversity in Mangalica pigs and their relationship to historical specimens. J. Anim. Breed. Genet. 130, 312320.

    • Search Google Scholar
    • Export Citation
  • 20.

    Olivieri, C., Marota, I., Rizzi, E., Ermini, L., Fusco, L., Pietrelli, A., De Bellis, G., Rollo, F., Luciani, S. (2014) Positioning the red deer (Cervus elaphus) hunted by the Tyrolean Iceman into a mitochondrial DNA phylogeny. PLoS ONE 9, e100136.

    • Search Google Scholar
    • Export Citation
  • 21.

    Pang, H., Liu, W., Chen, Y., Fang, L., Zhang, X., Cao, X. (2008) Identification of complete mitochondrial genome of the tufted deer. Mitochondrial DNA 19, 411417.

    • Search Google Scholar
    • Export Citation
  • 22.

    Pitra, C., Fickel, J., Meijaard, E., Groves, P. C. (2004) Evolution and phylogeny of old world deer. Mol. Phylogenet. Evol. 33, 880895.

    • Search Google Scholar
    • Export Citation
  • 23.

    Radko, A., Zalewski, D., Rubis, D., Szumec, A. (2014) Genetic differentiation among 6 populations of red deer (Cervus elaphus L.) in Poland based on microsatellite DNA polymorphism. Acta Biol. Hung. 65, 414427.

    • Search Google Scholar
    • Export Citation
  • 24.

    Sbisà, E., Tanzariello, F., Reyes, A., Pesole, G., Saccone, C. (1997) Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene 205, 125140.

    • Search Google Scholar
    • Export Citation
  • 25.

    Shao, Y., Su, W., Liu, H., Zha, D., Zhang, R., Xing, X. (2016) Complete mitochondrial genome sequence of northeastern red deer (Cervus elaphus xanthopygus). Mitochondrial DNA Early Online.

    • Search Google Scholar
    • Export Citation
  • 26.

    Shao, Y., Xing, X., Zha, D., Yang, F. (2016) Complete mitochondrial genome sequence of tarim red deer (Cervus elaphus yarkandensis). Mitochondrial DNA 547548.

    • Search Google Scholar
    • Export Citation
  • 27.

    Shao, Y., Zha, D., Xing, X., Su, W., Liu, H., Zhang, R. (2016) Complete mitochondrial genome sequence of northeastern sika deer (Cervus nippon hortulorum). Mitochondrial DNA 469470.

    • Search Google Scholar
    • Export Citation
  • 28.

    Skog, A., Zachos, F. E., Rueness, E. K., Feulner, P. G. D., Mysterud, A., Langvatn, R., Lorenzini, R., Hmwe, S. S., Lehoczky, I., Hartl, G. B., Stenseth, N. C., Jakobsen, K. S. (2009) Phylogeography of red deer (Cervus elaphus) in Europe. J. Biogeogr. 36, 6677.

    • Search Google Scholar
    • Export Citation
  • 29.

    Szabolcsi, Z., Egyed, B., Zenke, P., Pádár, Zs., Borsy, A., Stéger, V., Pásztor, E., Csányi, S., Buzás, Zs., Orosz, L. (2014) Constructing STR multiplexes for individual identification of Hungarian red deer. J. Forensic Sci. 59, 10901099.

    • Search Google Scholar
    • Export Citation
  • 30.

    Tamura, K., Dudley, J., Nei, M., Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 15961599.

    • Search Google Scholar
    • Export Citation
  • 31.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 27252729.

    • Search Google Scholar
    • Export Citation
  • 32.

    Wada, K., Nishibori, M., Yokohama, M. (2007) The complete nucleotide sequence of mitochondrial genome in Japanese Sika deer (Cervus nippon), and a phylogenetic analysis between Cervidae and Bovidae. Small Rum. Res. 69, 4654.

    • Search Google Scholar
    • Export Citation
  • 33.

    Wada, K., Okumura, K., Nishibori, M., Kikkawa, Y., Yokohama, M. (2010) The complete mitochondrial genome of the domestic red deer (Cervus elaphus) of New Zealand and its phylogenic position within the family Cervidae. Anim. Sci. J. 81, 551557.

    • Search Google Scholar
    • Export Citation
  • 34.

    Wang, Q., Yang, C. (2013) The phylogeny of the Cetartiodactyla based on complete mitochondrial genomes. Internat. J. Biol. 5, 3036.

  • 35.

    Yang, C., Li, P., Zhang, X., Guo, Y., Gao, Y., Xiong, Y., Wang, L., Qi, W., Yue, B. (2012) The complete mitochondrial genome of the Chinese Sika deer (Cervus nippon Temminck, 1838), and phylogenetic analysis among Cervidae, Moschidae and Bovidae. J. Nat. Hist. 46, 17471759.

    • Search Google Scholar
    • Export Citation
  • 36.

    Zachos, F. E., Hartl, G. B. (2011) Phylogeography, population genetics and conservation of the European red deer Cervus elaphus. Mammal Rev. 41, 138150.

    • Search Google Scholar
    • Export Citation
  • 37.

    Zhang, W-Q., Zhang, M-H. (2012) Phylogeny and evolution of Cervidae based on complete mitochondrial genomes. Genet. Mol. Res. 11, 628635.

    • Search Google Scholar
    • Export Citation
  • 38.

    Zsolnai, A., Lehoczky, I., Gyurmán, A., Nagy, J., Sugár, L., Anton, I., Horn, P., Magyary, I. (2009) Development of eight-plex microsatellite PCR for parentage control in deer. Archiv Tierzucht 52, 143149.

    • Search Google Scholar
    • Export Citation