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Comparative analysis of the complete mitochondrial genomes of two species of Clupeiformes and the phylogenetic implications for Clupeiformes

Published online by Cambridge University Press:  24 October 2022

Bingjian Liu
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Ying Peng
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Kun Zhang
College of Life Science, Hunan Normal University, Changsha, China
Yifan Liu
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Jiasheng Li
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Jian Chen
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Xuepeng Li
School of Ocean, Yantai University, Yantai, China
Xun Jin
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Sixu Zheng
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Yunpeng Wang
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Shufei Zhang
Guangdong Provincial Key Laboratory of Fishery Ecology and Environment, South China Sea Fisheries Research Institute, Chinese Academy of Fisheries Sciences, Guangzhou, Guangdong 510300, China
Li Gong
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Zhenming Lü
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Liqin Liu*
National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, Zhejiang Ocean University, 316022, Zhoushan, China
Author for correspondence: Liqin Liu, E-mail:


The mitochondrial genome provides important information for phylogenetic analysis and an understanding of evolutionary origin. In this study, the mitochondrial genomes of Ilisha elongata and Setipinna tenuifilis were sequenced, which are typical circular vertebrate mitochondrial genomes composed of 16,770 and 16,805 bp, respectively. The mitogenomes of I. elongata and S. tenuifilis include 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA), two ribosomal RNA (rRNA) genes and one control region (CR). Both two species' genome compositions were highly A + T biased and exhibited positive AT-skews and negative GC-skews. The genetic distance and Ka/Ks ratio analyses indicated that 13 PCGs were affected by purifying selection and the selection pressures were different from certain deep-sea fishes, which were most likely due to the difference in their living environment. Results of phylogenetic analysis support close relationships among Chirocentridae, Denticipitidae, Clupeidae, Engraulidae and Pristigasteridae based on the nucleotide and amino acid sequences of 13 PCGs. Within Clupeoidei, I. elongata and S. tenuifilis were most closely related to the family Pristigasteridae and Engraulidae, respectively. These results will help to better understand the evolutionary position of Clupeiformes and provide a reference for further phylogenetic research on Clupeiformes species.

Research Article
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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Bernt, M, Donath, A, Jühling, F, Externbrink, F, Florentz, C, Fritzsch, G, Pütz, J, Middendorf, M and Stadler, PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313319.Google ScholarPubMed
Blaber, SJM, Staunton, SJ, Milton, DA, Fry, G, Velde, TVD, Pang, J, Wong, P and Boon, TO (1998) The biology and life-history Strategies ofIlisha (Teleostei: Pristigasteridae) in the coastal waters and estuaries of Sarawak. Estuarine, Coastal and Shelf Science 47, 499511.CrossRefGoogle Scholar
Bloom, DD and Egan, JP (2018) Systematics of Clupeiformes and testing for ecological limits on species richness in a trans-marine/freshwater clade. Neotropical Ichthyology 16, e180095.CrossRefGoogle Scholar
Bloom, DD, Fikáček, M and Short, AEZ (2014) Clade age and diversification rate variation explain disparity in species richness among water scavenger beetle (Hydrophilidae) lineages. PLoS ONE 9, e98430.CrossRefGoogle ScholarPubMed
Boore, JL (1999) Animal mitochondrial genomes. Nucleic Acids Research 27, 17671780.CrossRefGoogle ScholarPubMed
Broughton, RE, Milam, JE and Roe, BA (2001) The complete sequence of the zebrafish (Danio rerio) mitochondrial genome and evolutionary patterns in vertebrate mitochondrial DNA. Genome Research 11, 19581967.CrossRefGoogle ScholarPubMed
Chen, D (1988) The biological characters of spawning population of I. elongata distributed in the coastal area off Shandong Province. Bulletin of Marine Science 7, 4955.Google Scholar
Chen, B and Zhang, CM (1993) Age and growth of mature individuals of I. elongata in the waters off Xiamen. Fujian Fish 4, 3538.Google Scholar
Cheng, Q and Zheng, B (1987) Systematic Synopsis of Chinese Fishes. Beijing, China: Science Press.Google Scholar
Comeron, JM and Aguadé, M (1998) An evaluation of measures of synonymous codon usage bias. Journal of Molecular Evolution 47, 268274.CrossRefGoogle ScholarPubMed
Fauron, CM and Wolstenholme, DR (1976) Structural heterogeneity of mitochondrial DNA molecules within the genus Drosophila. Proceedings of the National Academy of Sciences USA 73, 36233627.CrossRefGoogle ScholarPubMed
Grande, L (1985) Recent and fossil Clupeomorph Wshes with materials forrevision of the subgroups of Clupeoids. Bulletin of the American Museum of Natural History 181, 231372.Google Scholar
Greiner, S, Lehwark, P and Bock, R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research 47, W59W64.CrossRefGoogle ScholarPubMed
Habib, M, Lakra, WS, Mohindra, V, Khare, P, Barman, AS, Singh, A, Lal, KK, Punia, P and Khan, AA (2011) Evaluation of cytochrome b mtDNA sequences in genetic diversity studies of Channa marulius (Channidae: Perciformes). Molecular Biology Reports 38, 841846.CrossRefGoogle Scholar
Hall, T (1999) BioEdit: a user-friendly biological sequence alignment program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hatooka, K, Yamada, U, Aizawa, M, Yamaguchi, A and Yagishita, N (2013) Rajidae. Fishes of Japan with Pictorial Keys to the Species 3, 205216.Google Scholar
Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.Google Scholar
Inoue, JG, Miya, M, Tsukamoto, K and Nishida, M (2000) Complete mitochondrial DNA sequence of the Japanese sardine Sardinops melanostictus. Fisheries Science 66, 924932.CrossRefGoogle Scholar
Jia, C, Zhang, X, Xu, S, Yang, T and Gao, T (2020) Comparative analysis of the complete mitochondrial genomes of three rockfishes (Scorpaeniformes, Sebastiscus) and insights into the phylogenetic relationships of Sebastidae. Bioscience Reports 40, BSR20203379.CrossRefGoogle ScholarPubMed
Kartavtsev, YP, Jung, SO, Lee, YM, Byeon, HK and Lee, JS (2007) Complete mitochondrial genome of the bullhead torrent catfish, Liobagrus obesus (Siluriformes, Amblycipididae): genome description and phylogenetic considerations inferred from the Cyt b and 16S rRNA genes. Gene 396, 1327.CrossRefGoogle ScholarPubMed
Kim, JK, Choi, OI, Kim, JI, Chang, DS and Park, KD (2007) Age and growth of the elongate ilisha Ilisha elongata. Journal of Fisheries Science and Technology 10, 3036.Google Scholar
Kim, IC, Kweon, HS, Kim, YJ, Kim, CB, Gye, MC, Lee, WO, Lee, YS and Lee, JS (2004) The complete mitochondrial genome of the javeline goby Acanthogobius hasta (Perciformes, Gobiidae) and phylogenetic considerations. Gene 336, 147153.CrossRefGoogle ScholarPubMed
Lakra, WS, Goswami, M and Gopalakrishnan, A (2009) Molecular identification and phylogenetic relationships of seven Indian Sciaenids (Pisces: Perciformes, Sciaenidae) based on 16S rRNA and cytochrome c oxidase subunit I mitochondrial genes. Molecular Biology Reports 36, 831839.CrossRefGoogle ScholarPubMed
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 29472948.CrossRefGoogle ScholarPubMed
Lavoué, S, Miya, M, Inoue, JG, Saitoh, K and Nishida, M (2005) Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: implications for higher-level relationships within the Otocephala. Molecular Phylogenetics and Evolution 37, 165177.CrossRefGoogle ScholarPubMed
Lavoué, S, Miya, M, Musikasinthorn, P, Chen, WJ and Nishida, M (2013) Mitogenomic evidence for an Indo-West Pacific origin of the Clupeoidei (Teleostei: Clupeiformes). PLoS ONE 8, e56485.CrossRefGoogle Scholar
Lavoué, S, Miya, M and Nishida, M (2010) Mitochondrial phylogenomics of anchovies (family Engraulidae) and recurrent origins of pronounced miniaturization in the order Clupeiformes. Molecular Phylogenetics and Evolution 56, 480485.CrossRefGoogle ScholarPubMed
Lavoué, S, Miya, M, Saitoh, K, Ishiguro, NB and Nishida, M (2007) Phylogenetic relationships among anchovies, sardines, herrings and their relatives (Clupeiformes), inferred from whole mitogenome sequences. Molecular Phylogenetics and Evolution 43, 10961105.CrossRefGoogle Scholar
Li, Z, Wu, Q, Shan, X, Wang, X and Jin, X (2017) Interannual variations in fish community structure in the Bohai Sea. Journal of Fishery Sciences of China 24, 403413.CrossRefGoogle Scholar
Liu, HZ (2002) The structure and evolution of mitochondrial DNA control region of fish: focus on Acheilognathinae fish. Progress in Natural Science 3, 266270.Google Scholar
Liu, Z, Song, N, Yanagimoto, T, Han, Z, Shui, B and Gao, T (2017) Complete mitochondrial genome of three fish species (Perciformes: Amblyopinae): genome description and phylogenetic relationships. Pakistan Journal of Zoology 49, 107115.CrossRefGoogle Scholar
Lowe, T and Eddy, S (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955964.Google ScholarPubMed
Lu, X, Gong, L, Zhang, Y, Chen, J, Liu, L, Jiang, L, , Z, Liu, B, Tong, G and Wei, X (2020) The complete mitochondrial genome of Calappa bilineata: the first representative from the family Calappidae and its phylogenetic position within Brachyura. Genomics 112, 25162523.CrossRefGoogle ScholarPubMed
Meng, HZ, Yong, W and Jun, Z (2004) Studies on the growth and death character of Setipinna taty in the south of Bohai Sea. Journal of Zhejiang Ocean University 23, 3136.Google Scholar
Miya, M, Kawaguchi, A and Nishida, M (2001) 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 18, 19932009.CrossRefGoogle ScholarPubMed
Mongiardino Koch, N, Coppard, SE, Lessios, HA, Briggs, DEG, Mooi, R and Rouse, GW (2018) A phylogenomic resolution of the sea urchin tree of life. BMC Evolutionary Biology 18, 189.Google ScholarPubMed
Montagna, M, Chouaia, B, Sacchi, L, Porretta, D, Martin, E, Giorgi, A, Lozzia, GC and Epis, S (2014) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Environmental Entomology 43, 913922.CrossRefGoogle Scholar
Nekrutenko, A, Makova, KD and Li, WH (2002) The KA/KS ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genome Research 12, 198202.CrossRefGoogle Scholar
Nelson, GJ (1970) The Hyobranchial Apparatus of Teleostean Fishes of the Families Engraulidae and Chirocentridae. New York, NY: American Museum Museum novitates.Google Scholar
Nelson, JS, Grande, TC and Wilson, MV (2016) Fishes of the World. New York: John Wiley & Sons.CrossRefGoogle Scholar
Nielsen, R (2005) Molecular signatures of natural selection. Annual Review of Genetics 39, 197218.CrossRefGoogle ScholarPubMed
Ojala, D, Montoya, J and Attardi, G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290, 470474.CrossRefGoogle ScholarPubMed
Orešič, M and Shalloway, D (1998) Specific correlations between relative synonymous codon usage and protein secondary structure. Journal of Molecular Biology 281, 3148.CrossRefGoogle ScholarPubMed
Pavan, KA, Raman, S, Koringa, PG, Patel, N, Shah, T, Singh, RK, Krishna, G, Joshi, CG, Gireesh, BP and Chaudhari, A (2016) Complete mitochondrial genome of threatened mahseer Tor tor (Hamilton 1822) and its phylogenetic relationship within Cyprinidae family. Journal of Genetics 95, 111.Google Scholar
Peng, Z, Wang, J and He, S (2006) The complete mitochondrial genome of the helmet catfish Cranoglanis bouderius (Siluriformes: Cranoglanididae) and the phylogeny of otophysan fishes. Gene 376, 290297.CrossRefGoogle ScholarPubMed
Perna, NT and Kocher, TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41, 353358.Google ScholarPubMed
Rozas, J and Rozas, R (1995) DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetics parameters from DNA sequence data. Computer Applications in the Biosciences 11, 621625.Google ScholarPubMed
Saitoh, K, Miya, M, Inoue, JG, Ishiguro, NB and Nishida, M (2003) Mitochondrial genomics of ostariophysan fishes: perspectives on phylogeny and biogeography. Journal of Molecular Evolution 56, 464472.CrossRefGoogle ScholarPubMed
Sébastien, L, Bertrand, JA, Chen, WJ, Ho, HC, Motomura, H, Sado, T and Miya, M (2017) Phylogenetic position of the rainbow sardine Dussumieria (Dussumieriidae) and its bearing on the early evolution of the Clupeoidei. Gene 623, 4147.Google Scholar
Shen, X, Pu, Z, Chen, X, Murphy, RW and Shen, Y (2019) Convergent evolution of mitochondrial genes in deep-sea fishes. Frontiers in Genetics 10, 925.CrossRefGoogle ScholarPubMed
Singh, VK, Mangalam, AK, Dwivedi, S and Naik, S (1998) Primer premier: program for design of degenerate primers from a protein sequence. BioTechniques 24, 318319.CrossRefGoogle ScholarPubMed
Sudhir, K, Glen, S and Koichiro, T (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Sun, C-H, Zhang, Y-N, Zeng, X-S, Liu, D-W, Huang, Q, Zhang, X-L and Zhang, Q (2022) Mitogenome of Knodus borki (Cypriniformes: Characidae): genomic characterization and phylogenetic analysis. Molecular Biology Reports 49, 17411748.CrossRefGoogle ScholarPubMed
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564577.CrossRefGoogle ScholarPubMed
Wang, Q, Zhang, J, Matsumoto, H, Kim, JK and Li, C (2016) Population structure of elongate ilisha Ilisha elongata along the Northwestern Pacific Coast revealed by mitochondrial control region sequences. Fisheries Science 82, 771785.Google Scholar
Wei, SJ, Shi, M, Chen, XX, Sharkey, MJ, van Achterberg, C, Ye, GY and He, JH (2010) New views on strand asymmetry in insect mitochondrial genomes. PLoS ONE 5, e12708.Google ScholarPubMed
Whitehead, PJP (1985) Clupeoid Wshes of the World (Suborder Clupeoi-dei): An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf herrings. Part 1. Chirocen-tridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis 125, 1303.Google Scholar
Wiesemüller, B and Rothe, H (2006) Interpretation of bootstrap values in phylogenetic analysis. Anthropologischer Anzeiger 64, 161165.CrossRefGoogle ScholarPubMed
Xia, X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 15501552.CrossRefGoogle ScholarPubMed
Yamada, U, Tokimura, M, Horikawa, H and Nakabo, T (2007) Fishes and Fisheries of the East China and Yellow Seas. Kanagawa: Tokai University Press.Google Scholar
Yamaoka, K, Nakagawa, T and Uno, T (1978) Application of Akaike's Information Criterion (AIC) in the evaluation of linear pharmacokinetic equations. Journal of Pharmacokinetics and Biopharmaceutics 6, 165175.CrossRefGoogle ScholarPubMed
Yang, ZH (1998) Likelihood ratio tests for detecting positive selection and application to primate lyzosyme evolution. Molecular Biology and Evolution 15, 568573.CrossRefGoogle Scholar
Yang, Z and Bielawski, JP (2000) Statistical methods for detecting molecular adaptation. Trends in Ecology & Evolution 15, 496503.Google ScholarPubMed
Yang, R, Wu, X, Yan, P, Su, X and Yang, B (2010) Complete mitochondrial genome of Otis tarda (Gruiformes: Otididae) and phylogeny of Gruiformes inferred from mitochondrial DNA sequences. Molecular Biology Reports 37, 30573066.CrossRefGoogle ScholarPubMed
Yong, L, Jia, HC and Sheng, FLI (2004) A study on the distribution of Setipinna taty in the East China Sea. Marine Fisheries 26, 255260.Google Scholar
Zhang, LP, Cai, YY, Yu, DN, Storey, KB and Zhang, JY (2018) Gene characteristics of the complete mitochondrial genomes of Paratoxodera polyacantha and Toxodera hauseri (Mantodea: Toxoderidae). PeerJ 6, e4595.CrossRefGoogle Scholar
Zhang, D, Ding, G, Wang, G, Tang, B and Sun, H (2011) Structure and variable numbers of tandem repeats (VNTRs) of the mitochondrial control region in mitten crab Eriocheir (Crustacean: Brachyura). Molecular Biology Reports 38, 49354940.Google Scholar
Zhang, C, Zhang, K, Peng, Y, Zhou, J, Liu, Y and Liu, B (2022) Novel gene rearrangement in the mitochondrial genome of three Garra and insights into the phylogenetic relationships of Labeoninae. Frontiers in Genetics 13, 922634.CrossRefGoogle ScholarPubMed
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