Abstract
Within the order Testudines, while phylogenetic analyses have been performed on the suborder Cryptodira with complete mitochondrial genomes (mitogenomes), mitogenomic information from another important suborder Pleurodira has been inadequate. In the present study, complete mitochondrial DNA (mtDNA) sequences of two chelid turtles Chelodina rugosa and Chelus fimbriata were firstly determined, the lengths of which were 16,582 and 16,661 bp respectively. As the typical vertebrate mitogenome, both mtDNAs consist of 13 protein coding genes, 2 ribosomal RNAs (rRNAs), 22 transfer RNAs (tRNAs), and a long noncoding region (control region, CR). However, the initiation sites for light-strand replication (OL), which has been identified in all reported Cryptodire mitogenomes, were not found in the putative position of the two chelid turtles and African helmeted turtle Pelomedusa subrufa. The results suggested that the absence of mitogenomic initiation sites (OL) could be a characteristic of Pleurodira. Phylogenetic relationships of chelid turtles and other turtles were reconstructed using the reported mitogenomes. Both maximum likelihood (ML) and Bayesian inference (BI) analyses suggested the monophyly of Pleurodira and Cryptodira as well as a sister group relationship between the two chelid turtles with strong statistical support. This phylogenetic framework was also utilized to estimate divergence dates among lineages using relaxed-clock methods combined with fossil evidence. Divergence estimates revealed that genus Chelodina diverged from genus Chelus in Late Cretaceous (~83 million years ago (mya)), and the time is consistent with the vicariance of the fragments which was caused by Gondwana split.
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References
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780
Saccone C, De Giorgi C, Gissi C, Pesole G, Reyes A (1999) Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene 238:195–209
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, London
Macey JR, Larson A, Ananjeva NB, Fang Z, Papenfuss TJ (1997) Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol 14:91–104
Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376:163–165
Rhodin AGJ, van Dijk PP, Iverson JB, Shaffer HB (2010) Turtles of the world, 2010 update: annotated checklist of taxonomy and synonymy, distribution, and conservation status. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB, Mittermeier RA (eds) Conservation biology of freshwater turtles and tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs No. 5, pp 000.85–000.164. doi:10.3854/crm.5.000.checklist.v3.2010. http://www.iucn-tftsg.org/cbftt/
Kumazawa Y, Nishida M (1999) Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. Mol Biol Evol 16:784–792
Zhang L, Nie L, Cao C, Zhang Y (2008) The complete mitochondrial genome of the Keeled box turtle Pyxidea mouhotii and phylogenetic analysis of major turtle groups. J Genet Genomics 35:33–40
Peng QL, Nie LW, Pu YG (2006) Complete mitochondrial genome of Chinese big-headed turtle, Platysternon megacephalum, with a novel gene organization in vertebrate mtDNA. Gene 380:14–20
Parham JF, Feldman CR, Boore JL (2006) The complete mitochondrial genome of the enigmatic bigheaded turtle (Platysternon): description of unusual genomic features and the reconciliation of phylogenetic hypotheses based on mitochondrial and nuclear DNA. BMC Evol Biol 6:11
Gaffney ES (1986) Triassic and early Jurassic turtles. In: Padian K (ed) The beginnings of the age of dinosaurs. Cambridge, Cambridge University Press, pp 183–187
Gaffney ES, Jenkins FA Jr (2010) The cranial morphology of Kayentachelys, an Early Jurassic cryptodire, and the early history of turtles. Acta Zool 91:335–368
Pritchard PCH (1979) Piscivory in turtle and evolution of the long-necked chelidae In: Ferguson MWJ (ed) The structure, development and evolution of reptiles symposia of the Zoological Society of London no. 52. Academic Press, London, pp 87–110
Pritchard PCH, Trebbau P (1984) The turtle of Venezuela contributions to herpetology 2. Society for the Study of Amphibians and Reptiles. Oxford: Ohio Society for the Study of Amphibians and Reptiles
Burbidge AA, Kirsch JAW, Main AR (1974) Relationships within the Chelidae (Testudines: Pleurodira) of Australia and New Guinea. Copeia 1974:392–409
Lapparent de Broin Fd, Molnar R (2001) Eocene chelid turtles from Redbank Plains, Southeast Queensland, Australia. Geodiversitas 23:41–79
Gaffney ES (1977) The side-necked turtle family Chelidae: a theory of relationships using shared derived characters. Am Mus Novit 2620:1–28
Pritchard PCH (1984) Piscivory in turtles, and evolution of the long-necked Chelidae. Symp Zool Soc Lond 52:87–110
Seddon JM, Georges A, Baverstock PR, McCord W (1997) Phylogenetic relationships of chelid turtles (Pleurodira: Chelidae) based on mitochondrial 12S rRNA gene sequence variation. Mol Phylogenet Evol 7:55–61
Georoges A, Birrell J, Saint KM, McCord W, Donnellan SC (1999) A phylogeny for side-necked turtles (Chelonia: Pleurodira) based on mitochondrial and nuclear gene sequence variation. Biol J Linn Soc 67:213–246
Pollock DD, Eisen JA, Doggett NA, Cummings MP (2000) A case for evolutionary genomics and the comprehensive examination of sequence biodiversity. Mol Biol Evol 17:1776–1788
Zhang JF, Nie LW, Wang Y, Hu LL (2009) The complete mitochondrial genome of the large-headed frog, Limnonectes bannaensis (Amphibia: Anura), and a novel gene organization in the vertebrate mtDNA. Gene 442:119–127
Rui J, Wang Y, Nie L (2009) The complete mitochondrial DNA genome of Eremias brenchleyi (Reptilia: Lacertidae) and its phylogeny position within squamata reptiles. Amphib Reptil 30:25–35
Gu Z, Zhao X, Li N, Wu C (2007) Complete sequence of the yak (Bos grunniens) mitochondrial genome and its evolutionary relationship with other ruminants. Mol Phylogenet Evol 42:248–255
Yan J, Zhou K, Yang G (2005) Molecular phylogenetics of ‘river dolphins’ and the baiji mitochondrial genome. Mol Phylogenet Evol 37:743–750
Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
Thalman O, Hebler J, Poinar H (2004) Unreliable mtDNA due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol Ecol 13:321–335
Spinks P, Shaffer H (2007) Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conserv Genet 8:641–657
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25:955–964
Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, Watanabe K (1991) Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32:511–520
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Stamatakis A (2006) RAxML-VI-HPC: randomized axelerated maximum likelihood ver704 maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Huelsenbeck JP, Ronquist F (2005) MRBAYES: Bayesian inference of phylogenetic trees Version 312. Bioinformatics 17:754–755
Nylander JAA (2004) MrModeltest v2 Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Near JT, Meylan AP, Shaffer HB (2005) Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am Nat 165:137–146
Noonan BP, Chippindale PT (2006) Vicariant origin of Malagasy reptiles supports late cretaceous Antarctic land bridge. Am Nat 168:730–741
Albert EM, Mauro DS, García-París M, Rüber L, Zardoya R (2009) Effect of taxon sampling on recovering the phylogeny of squamate reptiles based on complete mitochondrial genome and nuclear gene sequence data. Gene 441:12–21
Shaffer HB (2009) Turtles (Testudines). In: Hedges SB, Kumar S (eds) The timetable of life. Oxford University Press, Oxford, pp 398–401
Meylan PA, Gaffney ES (1991) Araripemys Price, 1973. In: Maisey JF (ed) Santana fossils: an illustrated atlas. Tropical Fish Hobbyist Publications, Neptune, pp 326–334
Meylan PA, Moody RJT, Walker CA, Chapman SD (2000) Sandownia harrisi, a highly derived trionychoid turtle (Testudinata: Cryptodira) from the Early Cretaceous of the Isle Of Wright. J Vertebr Paleontol 20:522–532
Hutchison JH (1980) Turtle stratigraphy of the Willwood Formation, Wyoming: preliminary results. In: Gingerich PD (ed) Early Cenozoic paleontology and stratigraphy of the Bighorn Basin. University of Michigan Papers on Paleontology. 24:115–118
Huelsenbeck J, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913
Kumazawa Y, Ota H, Nishida M, Ozawa T (1998) The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions. Genetics 150:313–329
Saitoh K, Hayashizaki K, Yokoyama Y, Asahida T, Toyohara H, Yamashita Y (2000) Complete nucleotide sequence of Japanese flounder (Paralichthys olivaceus) mitochondrial genome: structural properties and cue for resolving teleostean relationships. J Hered 91:271–278
Zardoya R, Malaga-Trillo E, Veith M, Meyer A (2003) Complete nucleotide sequence of the mitochondrial genome of a salamander, Mertensiella luschani. Gene 317:17–27
Zardoya R, Meyer A (1998) Cloning and characterization of a microsatellite in the mitochondrial control region of the African side-necked turtle, Pelomedusa subrufa. Gene 216:149–153
Ojala DJ, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474
Boore JL (2001) Complete mitochondrial genome sequence of the polychaete annelid Platynereis dumerilii. Mol Biol Evol 18:1413–1416
Zardoya R, Meyer A (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci USA 95:14226–14231
Clayton DA (1982) Replication of animal mitochondrial DNA. Cell 28:693–705
Brennicke A, Clayton DA (1981) Nucleotide assignment of alkali-sensitive sites in mouse mitochondrial DNA. J Biol Chem 256:10613–10617
Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome A novel gene order in higher vertebrates. J Mol Biol 212:599–634
Seligmann H, Krishnan NM (2006) Mitochondrial replication origin stability and propensity of adjacent tRNA genes to form putative replication origins increase developmental stability in lizards. J Exp Zool B Mol Dev Evol 306:433–449
Seligmann HN, Krishnan M, Rao BJ (2006) Possible multiple origins of replication in primate mitochondria: alternative role of tRNA sequences. J Theor Biol 241:321–332
Pääbo S, Thomas WK, Whitfield KM, Kumazawa Y, Wilson AC (1991) Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol 33:426–430
Lee WJ, Kocher TD (1995) Complete sequence of a sea lamprey (Petromyzon marinus) mitochondrial genome: early establishment of the vertebrate genome organization. Genetics 139:873–887
Quinn TW, Mindell DI (1996) Mitochondrial gene order adjacent to the control region in crocodile, turtle, and tuatara. Mol Phylogenet Evol 5:344–351
Legler JM (1981) The taxonomy, distribution, and ecology of Australian freshwater turtles (Testudines: Pleurodira: Chelidae). Natl Geogr Soc Res Rep 13:391–404
Georges A, Adams M (1992) A phylogeny for Australian chelid turtles based on allozyme electrophoresis. Aust J Zool 49:453–476
Yanbin S (1998) A paleoisthmus linking southern South America with the Antarctic Peninsula during Late Cretaceous and Early Tertiary. Sci China D 41:225–229
Lawver LA, Dalziel IWD, Gahagan LM (1999) Antarctica keystone of Gondwana Animated presentation (June 25, 1999, 206 slides). University of Texas Institute for Geophysics. http://wwwigutexasedu/research/projects/plates/
Sanmartín I (2002) A paleogeographic history of the southern hemisphere. Private Publication, Uppsala
Veevers JJ, Powell CMcA, Roots SR (1991) Review of sea floors spreading around Australia. 1. Synthesis of the patterns of spreading. Aust J Earth Sci 38:373–389
Francis JE, Ashworth A, Cantrill DJ, Crame JA, Howe J, Stephens R, Tosolini A-M, Thorn V (2008) 100 million years of Antarctic climate evolution: evidence from fossil plants. In: Antarctica, a keystone in a changing world proceedings of the 10th international symposium on antarctic Earth sciences. The National Academies Press, Washington, pp 19–28
Elliot DH (1985) Physical geography-geological evolution. In: Bonner WN, Walton DWH (eds) Key environments: Antarctica. Pergamon, Oxford, pp 39–61
de la Fuente M, Lapparent de Broin Fd, Manera de Bianco T (2001) The oldest and first nearly complete skeleton of a chelid, of the Hydromedusa sub-group (Chelidae, Pleurodira), from the Upper Cretaceous of Patagonia. Bull Soc Geol Fr 172:237–244
Shaffer HB, Meylan P, McKnight ML (1997) Tests of turtle phylogeny: molecular, morphological, and paleontological approaches. Syst Biol 46:235–268
Krenz JG, Naylor GJ, Shaffer HB, Janzen FJ (2005) Molecular phylogenetics and evolution of turtles. Mol Phylogenet Evol 37:178–191
Barley AJ, Spinks PQ, Thomson RC, Shaffer HB (2010) Fourteen nuclear genes provide phylogenetic resolution for difficult nodes in the turtle tree of life. Mol Phylogenet Evol 55:1189–1194
Chandler CH, Janzen FJ (2009) The phylogenetic position of the snapping turtles (Chelydridae) base on nucleotide sequence data. Copeia 2:209–213
Thomson RC, Shaffer HB (2010) Sparse supermatrices for phylogenetic inference: taxonomy, alignment, rogue taxa, and the phylogeny of living turtles. Syst Biol 59:42–58
Hirayama R (1998) Oldest known sea turtle. Nature 392:705–708
Eaton JG, Cifelli RL, Hutchison JH, Kirkland JI, Parrish JM (1999) Cretaceous vertebrate faunas from the Kaiparowits Plateau, south-central Utah. In: Gillette DD (ed) Vertebrate paleontology in Utah. Utah Geological Survey, Miscellaneous Publication, Salt Lake City, pp 345–353
Nesov LA, Chkhikvadze VM (1987) New evidence on Paleocene turtle remains from South Kazakhstan. Bull Acad Sci Georgian SSR 125:177–180
Chkhikvadze VM (1990) The Paleogene turtles of USSR. Edition Metsniereba Publishers, Tbilisi, pp 1–95
Acknowledgments
This research was supported by the National Natural Science Foundation of China (NSFC, No. 30770296), the special fund for scientific research of Dr. authorized subjects in China (grant number 20080370001) and the Key Laboratory of Biotic Environment and Ecological Safety of Anhui province.
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Wang, L., Zhou, X., Nie, L. et al. The complete mitochondrial genome sequences of Chelodina rugosa and Chelus fimbriata (Pleurodira: Chelidae): implications of a common absence of initiation sites (OL) in pleurodiran turtles. Mol Biol Rep 39, 2097–2107 (2012). https://doi.org/10.1007/s11033-011-0957-1
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DOI: https://doi.org/10.1007/s11033-011-0957-1