The sequence and structure of the complete mtDNA control region (CR) of M. cephalus from African, Pacific, and Atlantic populations are presented in this study to assess its usefulness in phylogeographic studies of this species. The mtDNA CR sequence variations among M. cephalus populations largely exceeded intraspecific polymorphisms that are generally observed in other vertebrates. The length of CR sequence varied among M. cephalus populations due to the presence of indels and variable number of tandem repeats at the hypervariable domain. The high evolutionary rate of the CR in this species probably originated from these mutations. However, no excessive homoplasic mutations were noticed. Finally, the star shaped tree inferred from the CR polymorphism stresses a rapid radiation worldwide, in this species. The CR still appears as a good marker for phylogeographic investigations and additional worldwide samples are warranted to further investigate the genetic structure and evolution in M. cephalus. 1. Introduction The advent of next generation sequencing started an era of discovery for a wide array of genetic markers for population genetics, phylogeny, and so forth. However, we have only scratched the surface on the analyses of these new markers and most researchers still resort to using the mitochondrial DNA (mtDNA) for population and biodiversity studies. Furthermore, the nonrecombining nature due to maternal inheritance and fast evolution rate compared to the nuclear genome [1] makes mtDNA a popular marker for studying vertebrate population genetics [2–4]. Within the mitochondrial genome, evolutionary rates are highly variable among genes. For example, in salamanders, nucleotide substitution rates may range from 0.1 to 1 substitution/site/million years (MY) [5]. Among the coding genes, the cytochrome b (cyto b) and cytochrome oxidase I (COI) present the highest evolutionary rates; however, the noncoding region of the mitochondrial genome (i.e., the control region (CR)) evolves 2–5 times faster [6]. Because of this exceptionally high mutation rate characteristic, the CR was quickly considered of great utility for addressing intraspecific evolutionary questions [7, 8]. In Teleostei, the CR is located between and . Structurally, the CR is composed of a central conserved domain flanked by two highly variable (left and right) domains (Figure 1). In these large domains, several short (approximately <30？bp) but conserved sequenced blocks (CSBs) have been described and varied in occurrence between taxa [2]. In the central conserved domain, the CSB-D is
References
[1]
W. M. Brown, M. George Jr., and A. C. Wilson, “Rapid evolution of animal mitochondrial DNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 4, pp. 1967–1971, 1979.
[2]
W.-J. Lee, J. Conroy, W. H. Howell, and T. D. Kocher, “Structure and evolution of teleost mitochondrial control regions,” Journal of Molecular Evolution, vol. 41, no. 1, pp. 54–66, 1995.
[3]
C. L. Nesb？, M. O. Arab, and K. S. Jakobsen, “Heteroplasmy, length and sequence variation in mtDNA control regions of three percid fish species (Perca fluvatilis, P. nua, Stizostedion luciperca),” Genetics, vol. 148, no. 4, pp. 1907–1919, 1998.
[4]
M. Miya, A. Kawaguchi, and M. Nishida, “Mitogenomic exploration of higher teleostean phylogenies: a case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences,” Molecular Biology and Evolution, vol. 18, no. 11, pp. 1993–2009, 2001.
[5]
R. L. Mueller, “Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis,” Systematic Biology, vol. 55, no. 2, pp. 289–300, 2006.
[6]
A. Meyer, “Evolution of mitochondrial DNA in fishes,” in Biochemistry and Molecular Biology of Fishes. Molecular Biology Frontiers, P. W. Hochachka and T. P. Mommsen, Eds., vol. 2, pp. 1–38, Elsevier Science, Amsterdam, The Netherlands, 1993.
[7]
G. G. Brown, G. Gadaleta, G. Pepe, C. Saccone, and E. Sbisa, “Structural conservation and variation in the D-loop-containing region of vertebrate mitochondrial DNA,” Journal of Molecular Biology, vol. 192, no. 3, pp. 503–511, 1986.
[8]
S. R. Palumbi, “Nucleic Acids II: the polymerase chain reaction,” in Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Marble, Eds., pp. 205–247, Sinauer Associates Inc., 1996.
[9]
D. A. Clayton, “Replication and transcription of vertebrate mitochondrial DNA,” Annual Review of Cell Biology, vol. 7, pp. 453–478, 1991.
[10]
W. O. McMillan and S. R. Palumbi, “Rapid rate of control-region evolution in Pacific butterflyfishes (Chaetodontidae),” Journal of Molecular Evolution, vol. 45, no. 5, pp. 473–484, 1997.
[11]
L. Bernatchez, R. Guyomard, and F. Bonhomme, “DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations,” Molecular Ecology, vol. 1, no. 3, pp. 161–173, 1992.
[12]
A. P. Apostolidis, C. Triantaphyllidis, A. Kouvatsi, and P. S. Economidis, “Mitochondrial DNA sequence variation and phylogeography among Salmo trutta L. (Greek brown trout) populations,” Molecular Ecology, vol. 6, no. 6, pp. 531–542, 1997.
[13]
J. M. Thomson, “The grey mullets,” Oceanography and Marine Biology: An Annual Review, vol. 4, no. 1, pp. 301–335, 1966.
[14]
A. Rocha-Olivares, N. M. Garber, and K. C. Stuck, “High genetic diversity, large inter-oceanic divergence and historical demography of the striped mullet,” Journal of Fish Biology, vol. 57, no. 5, pp. 1134–1149, 2000.
[15]
A. Rocha-Olivares, N. M. Garber, A. F. Garber, and K. C. Stuck, “Structure of the mitochondrial control region and flanking tRNA genes of Mugil cephalus,” Hidrobiologica, vol. 15, no. 2, pp. 139–149, 2005.
[16]
B. W. Jamandre, J.-D. Durand, and W. N. Tzeng, “Phylogeography of the flathead mullet Mugil cephalus in the north-west Pacific as inferred from the mtDNA control region,” Journal of Fish Biology, vol. 75, no. 2, pp. 393–407, 2009.
[17]
F. Caldara, L. Bargelloni, L. Ostellari, E. Penzo, L. Colombo, and T. Patarnello, “Molecular phylogeny of grey mullets based on mitochondrial DNA sequence analysis: evidence of a differential rate of evolution at the intrafamily level,” Molecular Phylogenetics and Evolution, vol. 6, no. 3, pp. 416–424, 1996.
[18]
D. Crosetti, W. S. Nelson, and J. C. Avise, “Pronounced genetic structure of mitochondrial DNA among populations of the circumglobally distributed grey mullet (Mugil cephalus),” Journal of Fish Biology, vol. 44, no. 1, pp. 47–58, 1994.
[19]
A. R. Rossi, M. Capula, D. Crosetti, L. Sola, and D. E. Campton, “Allozyme variation in global populations of striped mullet, Mugil cephalus (Pisces: Mugilidae),” Marine Biology, vol. 131, no. 2, pp. 203–212, 1998.
[20]
E. Fraga, H. Schneider, M. Nirchio, E. Santa-Brigida, L. F. Rodrigues-Filho, and I. Sampaio, “Molecular phylogenetic analyses of mullets (Mugilidae, Mugiliformes) based on two mitochondrial genes,” Journal of Applied Ichthyology, vol. 23, no. 5, pp. 598–604, 2007.
[21]
S. Heras, M. I. Roldán, and M. G. Castro, “Molecular phylogeny of Mugilidae fishes revised,” Reviews in Fish Biology and Fisheries, vol. 19, no. 2, pp. 217–231, 2009.
[22]
J.-D. Durand, K.-N. Shen, W.-J. Chen et al., “Systematics of the grey mullets (Teleostei: Mugiliformes: Mugilidae): molecular phylogenetic evidence challenges two centuries of morphology-based taxonomy,” Molecular Phylogenetics and Evolution, vol. 64, no. 1, pp. 73–92, 2012.
[23]
K. Katoh, K. Misawa, K.-I. Kuma, and T. Miyata, “MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform,” Nucleic Acids Research, vol. 30, no. 14, pp. 3059–3066, 2002.
[24]
T. Golubchik, M. J. Wise, S. Easteal, and L. S. Jermiin, “Mind the gaps: evidence of bias in estimates of multiple sequence alignments,” Molecular Biology and Evolution, vol. 24, no. 11, pp. 2433–2442, 2007.
[25]
C.-S. Tzeng, C.-F. Hui, S.-C. Shen, and P. C. Huang, “The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates,” Nucleic Acids Research, vol. 20, no. 18, pp. 4853–4858, 1992.
[26]
R. G. Ravago, V. D. Monje, and M. A. Juinio-Me？ez, “Length and sequence variability in mitochondrial control region of the milkfish, Chanos chanos,” Marine Biotechnology, vol. 4, no. 1, pp. 40–50, 2002.
[27]
C. A. Chen, M. C. A. Ablan, J. W. McManus et al., “Variable numbers of tandem repeats (VNTRs), heteroplasmy, and sequence variation of the mitochondrial control region in the three-spot Dascyllus trimaculatus (Perciformes: Pomacentridae),” Zoological Studies, vol. 43, no. 4, pp. 803–812, 2004.
[28]
A. P. Takagi, S. Ishikawa, T. Nao et al., “Tandem repeat sequence segments in control region of bronze featherback Notopterus notopterus mitochondrial DNA,” Fisheries Science, vol. 72, no. 6, pp. 1319–1321, 2006.
[29]
M. Cervelli, M. Bianchi, M. Scalici, G. Gibertini, M. Oliverio, and P. Mariottini, “Length and sequence variation in the mitochondrialDNA control region of the Etruscan freshwater goby Padogobius nigricans (Teleostei, Gobiidae),” Journal of Fish Biology, vol. 71, pp. 141–147, 2007.
[30]
J.-L. Zhao, W.-W. Wang, S.-F. Li, and W.-Q. Cai, “Structure of the mitochondrial DNA control region of the Sinipercine fishes and their phylogenetic relationship,” Acta Genetica Sinica, vol. 33, no. 9, pp. 793–799, 2006.
[31]
D. L. Swofford, G. L. Olsen, P. J. Wadell, and D. M. Hillis, “Phylogenetic inference,” in Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Mable, Eds., pp. 407–514, Sinauer, Sunderland, Mass, USA, 1996.
[32]
S. Kumar, K. Tamura, and M. Nei, “MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment,” Briefings in Bioinformatics, vol. 5, no. 2, pp. 150–163, 2004.
[33]
J. P. Huelsenbeck and F. Ronquist, “MR-BAYES: Bayesian inference of phylogenetic trees,” Bioinformatics, vol. 17, no. 8, pp. 754–755, 2001.
[34]
D. Posada and K. A. Crandall, “Modeltest: testing the model of DNA substitution,” Bioinformatics, vol. 14, no. 9, pp. 817–818, 1998.
[35]
N. Billington and P. D. N. Hebert, “Mitochondrial DNA diversity in fishes and its implications for introductions,” Canadian Journal of Fisheries and Aquatic Sciences, vol. 48, no. 1, supplement, pp. 80–94, 1991.
[36]
J. L. Nielsen, M. C. Fountain, J. C. Favela, K. Cobble, and B. L. Jensen, “Oncorhynchus at the southern extent of their range: a study of mtDNA control-region sequence with special reference to an undescribed subspecies of O. mykiss from Mexico,” Environmental Biology of Fishes, vol. 51, no. 1, pp. 7–23, 1998.
[37]
A. Rocha-Olivares, R. H. Rosenblatt, and R. D. Vetter, “Cryptic species of rockfishes (Sebastes: Scorpaenidae) in the Southern Hemisphere inferred from mitochondrial lineages,” Journal of Heredity, vol. 90, no. 3, pp. 404–411, 1999.
[38]
S. Livi, L. Sola, and D. Crosetti, “Phylogeographic relationships among worldwide populations of the cosmopolitan marine species, the striped gray mullet (Mugil cephalus), investigated by partial cytochrome b gene sequences,” Biochemical Systematics and Ecology, vol. 39, no. 2, pp. 121–131, 2011.
[39]
T. C. Johnson, C. A. Scholz, M. R. Talbot et al., “Late pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes,” Science, vol. 273, no. 5278, pp. 1091–1093, 1996.
[40]
C. J. Allender, O. Seehausen, M. E. Knight, G. F. Turner, and N. Maclean, “Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14074–14079, 2003.
[41]
O. Seehausen, “African cichlid fish: a model system in adaptive radiation research,” Proceedings of the Royal Society B: Biological Sciences, vol. 273, no. 1597, pp. 1987–1998, 2006.
[42]
L. B. Beheregaray, P. Sunnucks, and D. A. Briscoe, “A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex,” Proceedings of the Royal Society B: Biological Sciences, vol. 269, no. 1486, pp. 65–73, 2002.
