Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Comparative mitogenomic analyses reveal cryptic diversity of the bryozoan Bugula neritina Linnaeus, 1758, in the Yellow Sea

Xin Shen A B C , Mei Tian A , Ka Hou Chu D , Jin Feng Wang C , Shuai Chen C , Hui Lian Liu E , Xiao Heng Zhao A and Fang Qing Zhao C F
+ Author Affiliations
- Author Affiliations

A Jiangsu Key Laboratory of Marine Biotechnology and Jiangsu Institute of Marine Resources, Huaihai Institute of Technology, Lianyungang 222005, P.R. China.

B Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Lianyungang 222000, P.R. China.

C Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, P.R. China.

D Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, NT, Hong Kong, Special Administrative Region, P.R. China.

E Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, P.R. China.

F Corresponding author. Email: zhfq@mail.biols.ac.cn

Marine and Freshwater Research 67(8) 1241-1252 https://doi.org/10.1071/MF15055
Submitted: 11 February 2015  Accepted: 24 June 2015   Published: 21 September 2015

Abstract

The bryozoan Bugula neritina Linnaeus, 1758, is known to be a complex of three cryptic species, namely Types S, D and N. In the present study, we determined the mitochondrial genomic features of B. neritina sampled from Qingdao (QD), China, and compared them with those of the genome reported for a specimen sampled from Taean Gun (TG), South Korea. The B. neritina QD mitochondrial genome has a duplication of trnL2 and lacks trnV compared with B. neritina TG. Five tRNAs (trnL1, trnA, trnE, trnY and trnV) are encoded on the light-strand of B. neritina TG mitochondrial genome, but only one tRNA (trnA) is identified on the B. neritina QD mitochondrial light strand. In contrast to the B. neritina TG mitochondrial genome, deletion of trnV and duplication of trnL2 are identified in the B. neritina QD mtDNA, and three tRNAs (trnE, trnL1 and trnY) exhibit translocation and inversion. The genetic distance in 12 protein-coding genes (PCGs) (amino acids) between the two B. neritina was 0.079, which is higher than interspecific values of 10 lophotrochozoan genera selected for comparison. All these results from comparison between the two B. neritina clearly indicate that they are genetically distinct species. Phylogenetic analysis based on cox1 and lrRNA sequences suggested that B. neritina TG belongs to the widely distributed Type S and B. neritina QD represents a new cryptic type closely related to Type N. This new type is designated as Type Y, for its occurrence in the Yellow Sea. The geographical range of the different types of B. neritina awaits further studies.

Additional keywords: genetic distance, gene rearrangement, mitogenome.


References

Abascal, F., Posada, D., and Zardoya, R. (2007). MtArt: a new model of amino acid replacement for Arthropoda. Molecular Biology and Evolution 24, 1–5.
MtArt: a new model of amino acid replacement for Arthropoda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFWgsA%3D%3D&md5=ad5ae8d3908b82561a3c277b2fdeac58CAS | 17043087PubMed |

Akasaki, T., Nikaido, M., Tsuchlya, K., Segawa, S., Hasegawa, M., and Okada, N. (2006). Extensive mitochondrial gene arrangements in coleoid Cephalopoda and their phylogenetic implications. Molecular Phylogenetics and Evolution 38, 648–658.
Extensive mitochondrial gene arrangements in coleoid Cephalopoda and their phylogenetic implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvVWnsL0%3D&md5=ce0072036b89d6ce36fd4140a8da8246CAS | 16442311PubMed |

Bandyopadhyay, P. K., Stevenson, B. J., Ownby, J. P., Cady, M. T., Watkins, M., and Olivera, B. M. (2008). The mitochondrial genome of Conus textile, coxI–coxII intergenic sequences and Conoidean evolution. Molecular Phylogenetics and Evolution 46, 215–223.
The mitochondrial genome of Conus textile, coxI–coxII intergenic sequences and Conoidean evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKgsQ%3D%3D&md5=c169aadc7c57a8822ff1fd238a61121cCAS | 17936021PubMed |

Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., and Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |

Boore, J. L. (2004). Complete mitochondrial genome sequence of Urechis caupo, a representative of the phylum Echiura. BMC Genomics 5, 67.
Complete mitochondrial genome sequence of Urechis caupo, a representative of the phylum Echiura.Crossref | GoogleScholarGoogle Scholar | 15369601PubMed |

Boore, J. L., and Brown, W. M. (1998). Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Current Opinion in Genetics & Development 8, 668–674.
Big trees from little genomes: mitochondrial gene order as a phylogenetic tool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1yisQ%3D%3D&md5=b8d46a3c8993a793da6c5283669b1dcaCAS |

Boore, J. L., Medina, M., and Rosenberg, L. A. (2004). Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis. Molecular Biology and Evolution 21, 1492–1503.
Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlKgtrY%3D&md5=8a242cfd80c717c1ac2253cfc55ae0bdCAS | 15014161PubMed |

Brauer, A., Kurz, A., Stockwell, T., Baden-Tillson, H., Heidler, J., Wittig, I., Kauferstein, S., Mebs, D., Stöcklin, R., and Remm, M. (2012). The mitochondrial genome of the venomous cone snail Conus consors. PLoS One 7, e51528.
The mitochondrial genome of the venomous cone snail Conus consors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2qtrzM&md5=033f51e32ff210067b51343ab9c0ab6bCAS | 23236512PubMed |

Breton, S., Burger, G., Stewart, D. T., and Blier, P. U. (2006). Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172, 1107–1119.
Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivFCkurk%3D&md5=8834a2f903fe192dbaad90eda119fcf9CAS | 16322521PubMed |

Burger, T. D., Shao, R. F., and Barker, S. C. (2014). Phylogenetic analysis of mitochondrial genome sequences indicates that the cattle tick, Rhipicephalus (Boophilus) microplus, contains a cryptic species. Molecular Phylogenetics and Evolution 76, 241–253.
Phylogenetic analysis of mitochondrial genome sequences indicates that the cattle tick, Rhipicephalus (Boophilus) microplus, contains a cryptic species.Crossref | GoogleScholarGoogle Scholar | 24685498PubMed |

Davidson, S. K., and Haygood, M. G. (1999). Identification of sibling species of the bryozoan Bugula neritina that produce different anticancer bryostatins and harbor distinct strains of the bacterial symbiont ‘Candidatus endobugula sertula’. The Biological Bulletin 196, 273–280.
Identification of sibling species of the bryozoan Bugula neritina that produce different anticancer bryostatins and harbor distinct strains of the bacterial symbiont ‘Candidatus endobugula sertula’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1Clurw%3D&md5=c8d31e37645b83aeffa60112fa7b2249CAS | 10390826PubMed |

Davidson, S. K., Allen, S. W., Lim, G. E., Anderson, C. M., and Haygood, M. G. (2001). Evidence for the biosynthesis of bryostatins by the bacterial symbiont ‘Candidatus Endobugula sertula’ of the bryozoan Bugula neritina. Applied and Environmental Microbiology 67, 4531–4537.
Evidence for the biosynthesis of bryostatins by the bacterial symbiont ‘Candidatus Endobugula sertula’ of the bryozoan Bugula neritina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1WisLw%3D&md5=ac2d959a86b6a085ffe5ce43b976161eCAS | 11571152PubMed |

Fehlauer-Ale, K. H., Mackie, J. A., Lim-Fong, G. E., Ale, E., Pie, M. R., and Waeschenbach, A. (2014). Cryptic species in the cosmopolitan Bugula neritina complex (Bryozoa, Cheilostomata). Zoologica Scripta 43, 193–205.
Cryptic species in the cosmopolitan Bugula neritina complex (Bryozoa, Cheilostomata).Crossref | GoogleScholarGoogle Scholar |

Gasser, R. B., Jabbar, A., Mohandas, N., Schnyder, M., Deplazes, P., Littlewood, D. T. J., and Jex, A. R. (2012). Mitochondrial genome of Angiostrongylus vasorum: comparison with congeners and implications for studying the population genetics and epidemiology of this parasite. Infection, Genetics and Evolution 12, 1884–1891.
Mitochondrial genome of Angiostrongylus vasorum: comparison with congeners and implications for studying the population genetics and epidemiology of this parasite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsF2rurfF&md5=41929f7f5797137aca74cdb24417fd52CAS | 22922297PubMed |

Griggio, F., Voskoboynik, A., Ianelli, F., Justy, F., Tilak, M.-K.,, Xavier, T., Pesole, G., Douzery, E. J. P., Mastrototaro, F., and Gissi, C. (2014). Ascidian mitogenomics: comparison of evolutionary rates in closely related taxa provides evidence of ongoing speciation events. Genome Biology and Evolution 6, 591–605.
Ascidian mitogenomics: comparison of evolutionary rates in closely related taxa provides evidence of ongoing speciation events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtlWrtLk%3D&md5=efae758975d2029b99a34176c715eff1CAS | 24572017PubMed |

Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=9a8bcb495d840a5a366c36fb50a050b7CAS | 20525638PubMed |

He, C. B., Wang, J., Gao, X. G., Song, W. T., Li, H. J., Li, Y. F., Liu, W. D., and Su, H. (2011). The complete mitochondrial genome of the hard clam Meretrix meretrix. Molecular Biology Reports 38, 3401–3409.
The complete mitochondrial genome of the hard clam Meretrix meretrix.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVGisLc%3D&md5=b8be03f6d74225ee043a67d89edf77f3CAS | 21086173PubMed |

Hebert, P. D., Stoeckle, M. Y., Zemlak, T. S., and Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology 2, e312.
Identification of birds through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 15455034PubMed |

Hickerson, M. J., Meyer, C. P., and Moritz, C. (2006). DNA barcoding will often fail to discover new animal species over broad parameter space. Systematic Biology 55, 729–739.
DNA barcoding will often fail to discover new animal species over broad parameter space.Crossref | GoogleScholarGoogle Scholar | 17060195PubMed |

Iannelli, F., Pesole, G., Sordino, P., and Gissi, C. (2007). Mitogenomics reveals two cryptic species in Ciona intestinalis. Trends in Genetics 23, 419–422.
Mitogenomics reveals two cryptic species in Ciona intestinalis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1agsro%3D&md5=c75ed63571dfb6be085f1cccce19ec62CAS | 17640763PubMed |

Jang, K. H., and Hwang, U. W. (2009). Complete mitochondrial genome of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata): phylogenetic position of Bryozoa and phylogeny of lophophorates within the Lophotrochozoa. BMC Genomics 10, 167.
Complete mitochondrial genome of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata): phylogenetic position of Bryozoa and phylogeny of lophophorates within the Lophotrochozoa.Crossref | GoogleScholarGoogle Scholar | 19379522PubMed |

Knudsen, B., Kohn, A. B., Nahir, B., McFadden, C. S., and Moroz, L. L. (2006). Complete DNA sequence of the mitochondrial genome of the sea-slug, Aplysia californica: conservation of the gene order in Euthyneura. Molecular Phylogenetics and Evolution 38, 459–469.
Complete DNA sequence of the mitochondrial genome of the sea-slug, Aplysia californica: conservation of the gene order in Euthyneura.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFCrtA%3D%3D&md5=42f2e2606d3894021c5394566152ec7eCAS | 16230032PubMed |

Krzywinski, J., Li, C., Morris, M., Conn, J. E., Lima, J. B., Povoa, M. M., and Wilkerson, R. C. (2011). Analysis of the evolutionary forces shaping mitochondrial genomes of a Neotropical malaria vector complex. Molecular Phylogenetics and Evolution 58, 469–477.
Analysis of the evolutionary forces shaping mitochondrial genomes of a Neotropical malaria vector complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFGksLY%3D&md5=1d7196b8486f7e43c3cf2e645773c04fCAS | 21241811PubMed |

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., and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=4f5bbb5dff6430062f29b590974bffceCAS | 17846036PubMed |

Lei, H., Zhou, X. F., Yang, Y., Xu, T., Yang, X., Sun, J., Yang, B., Hu, J., Lin, X., Long, L., and Liu, Y. (2010). Bryostatins from South China Sea bryozoan Bugula neritina L. Biochemical Systematics and Ecology 38, 1231–1233.
Bryostatins from South China Sea bryozoan Bugula neritina L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGhurc%3D&md5=0bff28dac68e7612d84c8324fdeadb11CAS |

Liu, X. X., Yin, X. M., and Ma, J. H. (2001). ‘Biology of Marine-fouling Bryozoans in the Coastal Waters of China.’ (Science Press: Beijing.)

Lohse, M., Drechsel, O., Kahlau, S., and Bock, R. (2013). OrganellarGenomeDRAW: a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research 41, W575–W581.
OrganellarGenomeDRAW: a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets.Crossref | GoogleScholarGoogle Scholar | 23609545PubMed |

Lopanik, N., Gustafson, K. R., and Lindquist, N. (2004). Structure of bryostatin 20: a symbiont-produced chemical defense for larvae of the host bryozoan, Bugula neritina. Journal of Natural Products 67, 1412–1414.
Structure of bryostatin 20: a symbiont-produced chemical defense for larvae of the host bryozoan, Bugula neritina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVeis78%3D&md5=af075b08a1b0bbbde16532182ec2ed75CAS | 15332866PubMed |

Mackie, J. A., Keough, M. J., and Christidis, L. (2006). Invasion patterns inferred from cytochrome oxidase I sequences in three bryozoans, Bugula neritina, Watersipora subtorquata, and Watersipora arcuata. Marine Biology 149, 285–295.
Invasion patterns inferred from cytochrome oxidase I sequences in three bryozoans, Bugula neritina, Watersipora subtorquata, and Watersipora arcuata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFGitLY%3D&md5=51b0cace4dda362effac3886bf011becCAS |

Manning, T. J., Land, M., Rhodes, E., Chamberlin, L., Rudloe, J., Phillips, D., Lam, T. T., Purcell, J., Cooper, H. J., Emmett, M. R., and Marshall, A. G. (2005). Identifying bryostatins and potential precursors from the bryozoan Bugula neritina. Natural Product Reports 19, 467–491.
Identifying bryostatins and potential precursors from the bryozoan Bugula neritina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFWqu7Y%3D&md5=b031e58b932a2ec7fa2e37cbe5013dadCAS |

Mao, M., Austin, A. D., Johnson, N. F., and Dowton, M. (2014). Coexistence of minicircular and a highly rearranged mtDNA molecule suggests that recombination shapes mitochondrial genome organization. Molecular Biology and Evolution 31, 636–644.
Coexistence of minicircular and a highly rearranged mtDNA molecule suggests that recombination shapes mitochondrial genome organization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsVSgt7w%3D&md5=5bdd01b9dcb9d51d304cc6c279ea1b68CAS | 24336845PubMed |

Maynard, B. T., Kerr, L. J., McKiernan, J. M., Jansen, E. S., and Hanna, P. J. (2005). Mitochondrial DNA sequence and gene organization in the Australian blacklip abalone Haliotis rubra (leach). Marine Biotechnology (New York, N.Y.) 7, 645–658.
Mitochondrial DNA sequence and gene organization in the Australian blacklip abalone Haliotis rubra (leach).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GlsbjP&md5=49230296d3f7c6939ee2b969d0779766CAS |

McGovern, T. M., and Hellberg, M. E. (2003). Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina. Molecular Ecology 12, 1207–1215.
Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlSqs7Y%3D&md5=a7e44f8203674e3f3c1768d58232c1e8CAS | 12694284PubMed |

Medina, M., Lal, S., Valles, Y., Takaoka, T. L., Dayrat, B. A., Boore, J. L., and Gosliner, T. (2011). Crawling through time: transition of snails to slugs dating back to the Paleozoic, based on mitochondrial phylogenomics. Marine Genomics 4, 51–59.
Crawling through time: transition of snails to slugs dating back to the Paleozoic, based on mitochondrial phylogenomics.Crossref | GoogleScholarGoogle Scholar | 21429465PubMed |

Meng, X., Shen, X., Zhao, N., Tian, M., Liang, M., Hao, J., Cheng, H., Yan, B., Dong, Z., and Zhu, X. (2013). Mitogenomics reveals two subspecies in Coelomactra antiquata (Mollusca: Bivalvia). Mitochondrial DNA 24, 102–104.
Mitogenomics reveals two subspecies in Coelomactra antiquata (Mollusca: Bivalvia).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFaktb8%3D&md5=6857e09fe0d3e339fd79f7de7795d43bCAS | 23025478PubMed |

Mizi, A., Zouros, E., Moschonas, N., and Rodakis, G. C. (2005). The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: Implications for the doubly uniparental inheritance mode of mtDNA. Molecular Biology and Evolution 22, 952–967.
The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: Implications for the doubly uniparental inheritance mode of mtDNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFaisLo%3D&md5=97a4fffb0b1b6efd925deb706559ddb4CAS | 15647523PubMed |

Neiman, M., Hehman, G., Miller, J. T., Logsdon, J. M., and Taylor, D. R. (2010). Accelerated mutation accumulation in asexual lineages of a freshwater snail. Molecular Biology and Evolution 27, 954–963.
Accelerated mutation accumulation in asexual lineages of a freshwater snail.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjslals7k%3D&md5=44d92a3584be321938eb805dd615275cCAS | 19995828PubMed |

Nesnidal, M. P., Helmkampf, M., Bruchhaus, I., and Hausdorf, B. (2011). The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata): compositional bias affects phylogenetic analyses of lophotrochozoan relationships. BMC Genomics 12, 572.
The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata): compositional bias affects phylogenetic analyses of lophotrochozoan relationships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFyksLw%3D&md5=5fa59e836812d3f6e22a6e390304db0eCAS | 22111761PubMed |

Nikulina, E. A., Hanel, R., and Schafer, P. (2007). Cryptic speciation and paraphyly in the cosmopolitan bryozoan Electra pilosa-impact of the Tethys closing on species evolution. Molecular Phylogenetics and Evolution 45, 765–776.
Cryptic speciation and paraphyly in the cosmopolitan bryozoan Electra pilosa-impact of the Tethys closing on species evolution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2snptFeqsA%3D%3D&md5=7f27e9c7bd7d75368674197474729614CAS | 17920936PubMed |

Perna, N. T., and Kocher, T. D. (1995). Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353–358.
Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnslWnt7g%3D&md5=dac6c0df1cd988717bf4b7555b59fa80CAS | 7563121PubMed |

Ren, J. F., Shen, X., Sun, M. A., Jiang, F., Yu, Y., Chi, Z. F., and Liu, B. (2009). The complete mitochondrial genome of the clam Meretrix petechialis (Mollusca: Bivalvia: Veneridae). Mitochondrial DNA 20, 78–87.
The complete mitochondrial genome of the clam Meretrix petechialis (Mollusca: Bivalvia: Veneridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFKrsrY%3D&md5=596da7cfacf54c61f95e12b93c4f8579CAS |

Ren, J. F., Liu, X., Jiang, F., Guo, X. M., and Liu, B. (2010). Unusual conservation of mitochondrial gene order in Crassostrea oysters: evidence for recent speciation in Asia. BMC Evolutionary Biology 10, 394.
Unusual conservation of mitochondrial gene order in Crassostrea oysters: evidence for recent speciation in Asia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFWgtw%3D%3D&md5=47aa5b0148c815b4d37930b3b599946aCAS |

Robinson, N. A., Hall, N. E., Ross, E. M., Cooke, I. R., Shiel, B. P., Robinson, A. J., and Strugnell, J. M. (2014). The complete mitochondrial genome of Haliotis laevigata (Gastropoda: Haliotidae) using MiSeq and HiSeq sequencing. Mitochondrial DNA , .
The complete mitochondrial genome of Haliotis laevigata (Gastropoda: Haliotidae) using MiSeq and HiSeq sequencing.Crossref | GoogleScholarGoogle Scholar | 24660910PubMed |

Schattner, P., Brooks, A. N., and Lowe, T. M. (2005). The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Research 33, W686–W689.
The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslyrt7c%3D&md5=597b64b36ca7d2e4c0bbf85e63c33570CAS | 15980563PubMed |

Schwaninger, H. R. (2008). Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea L. (Cheilostomata): another cryptic marine sibling species complex? Molecular Phylogenetics and Evolution 49, 893–908.
Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea L. (Cheilostomata): another cryptic marine sibling species complex?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCntLzK&md5=3fa5b6201bf239cff69b9b3103853b64CAS | 18799135PubMed |

Sharp, K. H., Davidson, S. K., and Haygood, M. G. (2007). Localization of ‘Candidatus Endobugula sertula’ and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. The ISME Journal 1, 693–702.
Localization of ‘Candidatus Endobugula sertula’ and the bryostatins throughout the life cycle of the bryozoan Bugula neritina.Crossref | GoogleScholarGoogle Scholar | 18059493PubMed |

Shen, X., Tian, M., Meng, X. P., Liu, H. L., Cheng, H. L., Zhu, C. B., and Zhao, F. Q. (2012). Complete mitochondrial genome of Membranipora grandicella (Bryozoa: Cheilostomatida) determined with next-generation sequencing: the first representative of the suborder Malacostegina. Comparative Biochemistry and Physiology – Part D 7, 248–253.
| 1:CAS:528:DC%2BC38XlsFCrtrg%3D&md5=c66f00c3958b31c67858feec6341d0dbCAS |

Shen, X., Meng, X. P., Chu, K. H., Zhao, N. N., Tian, M., Liang, M., and Hao, J. (2014). Comparative mitogenomic analysis reveals cryptic species: a case study in Mactridae (Mollusca: Bivalvia). Comparative Biochemistry and Physiology – Part D 12, 1–9.
| 1:CAS:528:DC%2BC2cXhsFWgsL%2FK&md5=7b0d603249dc43306394fe459bbbe935CAS |

Simpson, J. T., Wong, K., Jackman, S. D., Schein, J. E., Jones, S. J. M., and Birol, I. (2009). ABySS: a parallel assembler for short read sequence data. Genome Research 19, 1117–1123.
ABySS: a parallel assembler for short read sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGrsbo%3D&md5=78069461cb83c02e41635b8add4147f8CAS | 19251739PubMed |

Sun, M. A., Wu, Z. G., Shen, X., Ren, J. F., Liu, X. X., Liu, H. L., and Liu, B. (2009). The complete mitochondrial genome of Watersipora subtorquata (Bryozoa, Gymnolaemata, Ctenostomata) with phylogenetic consideration of Bryozoa. Gene 439, 17–24.
The complete mitochondrial genome of Watersipora subtorquata (Bryozoa, Gymnolaemata, Ctenostomata) with phylogenetic consideration of Bryozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1eksLk%3D&md5=8095c360188d286228227560bb7f00c7CAS |

Sun, M. A., Shen, X., Liu, H. L., Liu, X. X., Wu, Z. G., and Liu, B. (2011). Complete mitochondrial genome of Tubulipora flabellaris (Bryozoa: Stenolaemata): the first representative from the class Stenolaemata with unique gene order. Marine Genomics 4, 159–165.
Complete mitochondrial genome of Tubulipora flabellaris (Bryozoa: Stenolaemata): the first representative from the class Stenolaemata with unique gene order.Crossref | GoogleScholarGoogle Scholar |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=e8c149c24c63ea752681aeac2f06680fCAS | 24132122PubMed |

Van Wormhoudt, A., Le Bras, Y., and Huchette, S. (2009). Haliotis marmorata from Senegal; a sister species of Haliotis tuberculata: morphological and molecular evidence. Biochemical Systematics and Ecology 37, 747–755.
Haliotis marmorata from Senegal; a sister species of Haliotis tuberculata: morphological and molecular evidence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGnsbc%3D&md5=ab4b0621397a27c92c926dc12b47e185CAS |

Veale, A. J., Williams, L., Tsai, P., Thakur, V., and Lavery, S. (2014). The complete mitochondrial genomes of two chiton species (Sypharochiton pelliserpentis and Sypharochiton sinclairi) obtained using Illumina next generation sequencing. Mitochondrial DNA , .
The complete mitochondrial genomes of two chiton species (Sypharochiton pelliserpentis and Sypharochiton sinclairi) obtained using Illumina next generation sequencing.Crossref | GoogleScholarGoogle Scholar | 24708108PubMed |

Waeschenbach, A., Telford, M. J., Porter, J. S., and Littlewood, D. T. J. (2006). The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa. Molecular Phylogenetics and Evolution 40, 195–207.
The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvF2nuro%3D&md5=b2fb32209017029e55e5b62d9eb99a5cCAS | 16621614PubMed |

Waeschenbach, A., Porter, J. S., and Hughes, R. N. (2012). Molecular variability in the Celleporella hyalina (Bryozoa; Cheilostomata) species complex: evidence for cryptic speciation from complete mitochondrial genomes. Molecular Biology Reports 39, 8601–8614.
Molecular variability in the Celleporella hyalina (Bryozoa; Cheilostomata) species complex: evidence for cryptic speciation from complete mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyksL%2FF&md5=169b56786c1ab894b4772ecd28464ed7CAS | 22714911PubMed |

Wang, H. X., Zhang, S. P., Li, Y., and Liu, B. Z. (2010). Complete mtDNA of Meretrix lusoria (Bivalvia: Veneridae) reveals the presence of an atp8 gene, length variation and heteroplasmy in the control region. Comparative Biochemistry and Physiology – Part D 5, 256–264.

Wang, M., Sun, S., Li, C., and Shen, X. (2011). Distinctive mitochondrial genome of calanoid copepod Calanus sinicus with multiple large non-coding regions and reshuffled gene order: useful molecular markers for phylogenetic and population studies. BMC Genomics 12, 73.
Distinctive mitochondrial genome of calanoid copepod Calanus sinicus with multiple large non-coding regions and reshuffled gene order: useful molecular markers for phylogenetic and population studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVKmtLs%3D&md5=ef9922822c7e2c5bfac8d9391725c615CAS |

Wang, W., Guo, B., Li, J., Wang, H., Qi, P., Lv, Z., and Wu, C. (2013). Complete mitochondrial genome of the spineless cuttlefish Sepiella inermis (Sepioidea, Sepiidae). Mitochondrial DNA 26, 151–152.
| 24006867PubMed |

Wei, M., Yang, S., Yu, P., and Wan, Q. (2014). The complete mitochondrial genome of Hyriopsis cumingii (Unionoida: Unionidae): genome description and related phylogenetic analyses. Mitochondrial DNA , .
| 25329293PubMed |

Wu, Z. G., Shen, X., Sun, M. A., Ren, J. F., Wang, Y. J., Huang, Y. L., and Liu, B. (2009). Phylogenetic analyses of complete mitochondrial genome of Urechis unicinctus (Echiura) support that echiurans are derived annelids. Molecular Phylogenetics and Evolution 52, 558–562.
Phylogenetic analyses of complete mitochondrial genome of Urechis unicinctus (Echiura) support that echiurans are derived annelids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12htrk%3D&md5=820a824af513143ecd5b8feb1be3ff29CAS |

Wyman, S. K., Jansen, R. K., and Boore, J. L. (2004). Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20, 3252–3255.
Automatic annotation of organellar genomes with DOGMA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSrur%2FJ&md5=d67b870aabc17e3a0fa585b604911724CAS | 15180927PubMed |