Abstract
Heteroconchia, a widespread and abundant aquatic invertebrate, is an important clade of bivalve mollusks. The relationship between the three branches of Heteroconchia, Palaeoheterodonta, Archiheterodonta, and Euheterodonta has become a main controversy in molecular studies of the relationships between bivalves. In the present study, we assembled the complete mitochondrial genomes of Tapes dorsatus (Veneridae) and Cardita variegata (Carditidae) using high-throughput sequencing. C. variegata is the first mitochondrial genome belonging to the family Carditidae to be reported. We used 12 protein coding genes (excluding atp8) from the complete mitochondrial genomes of 146 species to recover the internal relationships of Heteroconchia. Our results support the traditional view of early branching of Palaeoheterodonta and the recovery of the monophyly of Palaeoheterodonta, Anomalodesmata, Imparidentia. Rearrangement analysis show that gene arrangement within Venerida was highly variable. Time-calibrated phylogenetic studies based on a relaxed molecular clock model suggested that Veneridae originated approximately 337.62 million years ago (Ma) and split into two major clades, whereas Carditidae originated approximately 510.09 Ma. Our results provide evidence of the internal relationships of Heteroconchia.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Data Availability Statement
The genome sequence data that support the findings of this study are openly available in GenBank of NCBI at (https://www.ncbi.nlm.nih.gov/nuccore/OP066992, https://www.ncbi.nlm.nih.gov/nuccore/OP021896) under the accession number: OP066992, OP021896.
References
Bieler R, Mikkelsen P M. 2006. Bivalvia—a look at the branches. Zoological Journal of the Linnean Society, 148(3): 223–235, https://doi.org/10.1111/j.1096-3642.2006.00255.x.
Bieler R, Mikkelsen P M, Collins T M et al. 2014. Investigating the bivalve tree of life—an exemplar-based approach combining molecular and novel morphological characters. Invertebrate Systematics, 28(1): 32–115, https://doi.org/10.1071/IS13010.
Bolotov I N, Kondakov A V, Vikhrev I V et al. 2017. Ancient river inference explains exceptional Oriental freshwater mussel radiations. Scientific Reports, 7(1): 2135, https://doi.org/10.1038/s41598-017-02312-z.
Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767–1780, https://doi.org/10.1093/nar/27.8.1767.
Boore J L, Medina M, 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(8): 1492–1503, https://doi.org/10.1093/molbev/msh090.
Chavan A. 1969. Superfamily Carditacea Fleming, 1820. Geological Society of America & University of Kansas Press, Boulder, Colorado & Lawrence, Kansas, America. p.N543–N561.
Canapa A, Marota I, Rollo F et al. 1996. Phylogenetic analysis of Veneridae (Bivalvia): comparison of molecular and palaeontological data. Journal of Molecular Evolution, 43(5): 517–522, https://doi.org/10.1007/BF02337522.
Canapa A, Schiaparelli S, Marota I et al. 2003. Molecular data from the 16S rRNA gene for the phylogeny of Veneridae (Mollusca: Bivalvia). Marine Biology, 142(6): 1125–1130, https://doi.org/10.1007/s00227-003-1048-1.
Chen A H, Li Z X, Feng G N. 2009. Phylogenetic relationships of the genus Meretrix (Mollusca: Veneridae) based on mitochondrial COI gene sequences. Zoological Research, 30(3): 233–239, https://doi.org/10.3724/SP.J.1141.2009.03233.
Coan E V. 1977. Preliminary review of the northwest American Carditidae. The Veliger, 19(4): 375–386.
Cope J C W. 2002. Diversification and biogeography of bivalves during the Ordovician Period. Geological Society, London, Special Publications, 194(1): 35–52, https://doi.org/10.1144/GSL.SP.2002.194.01.04.
Cope J C W. 2004. Bivalve and rostroconch mollusks. In: Webby B, Paris F, Droser M et al eds. The Great Ordovician Biodiversification Event. Columbia University Press, New York. p.196–208.
Dall W H. 1903. Synopsis of the Carditacea and of the American species. Proceedings of the Academy of Natural Sciences of Philadelphia, 54(3): 696–716, http://www.jstor.org/stable/4062722. Accessed on 2023-10-16.
Dreyer H, Steiner G. 2006. The complete sequences and gene organisation of the mitochondrial genomes of the heterodont bivalves Acanthocardia tuberculata and Hiatella arctica—and the first record for a putative Atp ase subunit 8 gene in marine bivalves. Frontiers in Zoology, 3: 13, https://doi.org/10.1186/1742-9994-3-13.
Fang Z J, Chen J H, Chen C Z et al. 2009. Supraspecific taxa of the Bivalvia first named, described, and published in China (1927–2007). The University of Kansas Paleontological Contributions, New Series, 17: 1–157, https://doi.org/10.17161/PCNS.1808.7949.
Feng J T, Guo Y H, Yan C R et al. 2021. Novel gene rearrangement in the mitochondrial genome of Siliqua minima (Bivalvia, Adapedonta) and phylogenetic implications for Imparidentia. PLoS One, 16(4): e0249446, https://doi.org/10.1371/journal.pone.0249446.
Giribet G, Wheeler W. 2002. On bivalve phylogeny: a highlevel analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebrate Biology, 121(4): 271–324, https://doi.org/10.1111/j.1744-7410.2002.tb00132.x.
Gissi C, Iannelli F, Pesole G. 2008. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity, 101(4): 301–320, https://doi.org/10.1038/hdy.2008.62.
Gonzalez V L, Andrade S C S, Bieler R et al. 2015. A phylogenetic backbone for Bivalvia: an RNA-seq approach. Proceedings of the Royal Society B: Biological Sciences, 282(1801): 20142332, https://doi.org/10.1098/rspb.2014.2332.
Graf D L, Jones H, Geneva A J et al. 2015. Molecular phylogenetic analysis supports a Gondwanan origin of the Hyriidae (Mollusca: Bivalvia: Unionida) and the paraphyly of Australasian taxa. Molecular Phylogenetics and Evolution, 85: 1–9, https://doi.org/10.1016/j.ympev.2015.01.012.
Grande C, Templado J, Zardoya R. 2008. Evolution of gastropod mitochondrial genome arrangements. BMC Evolutionary Biology, 8(1): 61, https://doi.org/10.1186/1471-2148-8-61.
Hu P, Wang R J. 2019. The complete mitochondrial genome of Parantica sita sita (Lepidoptera: Nymphalidae: Danainae) revealing substantial genetic divergence from its sibling subspecies P. s. niphonica. Gene, 686: 76–84, https://doi.org/10.1016/j.gene.2018.10.088.
Huang X C, Wu R W, An C T et al. 2018. Reclassification of Lamprotula rochechouartii as Margaritifera rochechouartii comb. nov. (Bivalvia: Margaritiferidae) revealed by time-calibrated multi-locus phylogenetic analyses and mitochondrial phylogenomics of Unionoida. Molecular Phylogenetics and Evolution, 120: 297–306, https://doi.org/10.1016/j.ympev.2017.12.017.
Huber M. 2010. Compendium of Bivalves. A Full-Color Guide to 3,300 of the World’s Marine Bivalves. A Status on Bivalvia after 250 Years of Research. ConchBooks, Hackenheim, Germany. 901p.
Johnson S B, Krylova E M, Audzijonyte A et al. 2017. Phylogeny and origins of chemosynthetic vesicomyid clams. Systematics and Biodiversity, 15(4): 346–360, https://doi.org/10.1080/14772000.2016.1252438.
Kalyaanamoorthy S, Minh B Q, Wong T K F et al. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587–589, https://doi.org/10.1038/nmeth.4285.
Kappner I, Bieler R. 2006. Phylogeny of Venus clams (Bivalvia: Venerinae) as inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution, 40(2): 317–331, https://doi.org/10.1016/j.ympev.2006.02.006.
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4): 772–780, https://doi.org/10.1093/molbev/mst010.
Kong L F, Li Y N, Kocot K M et al. 2020. Mitogenomics reveals phylogenetic relationships of Arcoida (Mollusca, Bivalvia) and multiple independent expansions and contractions in mitochondrial genome size. Molecular Phylogenetics and Evolution, 150: 106857, https://doi.org/10.1016/j.ympev.2020.106857.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7): 1870–1874, https://doi.org/10.1093/molbev/msw054.
Lee Y, Kwak H, Shin J et al. 2019. A mitochondrial genome phylogeny of Mytilidae (Bivalvia: Mytilida). Molecular Phylogenetics and Evolution, 139: 106533, https://doi.org/10.1016/j.ympev.2019.106533.
Lemer S, Bieler R, Giribet G. 2019. Resolving the relationships of clams and cockles: dense transcriptome sampling drastically improves the bivalve tree of life. Proceedings of the Royal Society B: Biological Sciences, 286(1896): 20182684, https://doi.org/10.1098/rspb.2018.2684.
Letunic I, Bork P. 2021. Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49(W1): W293–W296, https://doi.org/10.1093/nar/gkab301.
Lohse M, Drechsel O, Bock R. 2007. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics, 52(5–6): 267–274, https://doi.org/10.1007/s00294-007-0161-y.
Meng X P, Shen X, Zhao N N et al. 2013. The complete mitochondrial genome of the clam Mactra veneriformis (Bivalvia: Mactridae): has a unique non-coding region, missing atp8 and typical tRNASer. Mitochondrial DNA, 24(6): 613–615, https://doi.org/10.3109/19401736.2013.772152.
Mikkelsen N T, Kocot K M, Halanych K M. 2018. Mitogenomics reveals phylogenetic relationships of caudofoveate aplacophoran molluscs. Molecular Phylogenetics and Evolution, 127: 429–436, https://doi.org/10.1016/j.ympev.2018.04.031.
Milbury C A, Gaffney P M. 2005. Complete mitochondrial DNA sequence of the eastern oyster Crassostrea virginica. Marine Biotechnology, 7(6): 697–712, https://doi.org/10.1007/s10126-005-0004-0.
Minh B Q, Schmidt H A, Chernomor O et al. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37(5): 1530–1534, https://doi.org/10.1093/molbev/msaa015.
Monari S. 2009. Phylogeny and biogeography of pholadid bivalve Barnea (Anchomasa) with considerations on the phylogeny of Pholadoidea. Acta Palaeontologica Polonica, 54(2): 315–335, https://doi.org/10.4202/app.2008.0068.
Osigus H J, Eitel M, Bernt M et al. 2013. Mitogenomics at the base of Metazoa. Molecular Phylogenetics and Evolution, 69(2): 339–351, https://doi.org/10.1016/j.ympev.2013.07.016.
Passamonti M, Mantovani B, Scali V. 1999. Allozymic analysis of some Mediterranean Veneridae (Mollusca: Bivalvia): preliminary notes on taxonomy and systematics of the family. Journal of the Marine Biological Association of the United Kingdom, 79(5): 899–906, https://doi.org/10.1017/S0025315498001064.
Pérez D E. 2019. Phylogenetic relationships of the family Carditidae (Bivalvia: Archiheterodonta). Journal of Systematic Palaeontology, 17(16): 1359–1395, https://doi.org/10.1080/14772019.2018.1532463.
Plazzi F, Passamonti M. 2010. Towards a molecular phylogeny of Mollusks: bivalves’ early evolution as revealed by mitochondrial genes. Molecular Phylogenetics and Evolution, 57(2): 641–657, https://doi.org/10.1016/j.ympev.2010.08.032.
Podsiadlowski L, Braband A, Mayer G. 2008. The complete mitochondrial genome of the onychophoran Epiperipatus biolleyi reveals a unique transfer RNA set and provides further support for the Ecdysozoa hypothesis. Molecular Biology and Evolution, 25(1): 42–51, https://doi.org/10.1093/molbev/msm223.
Rahuman S, Jeena N S, Asokan P K et al. 2020. Mitogenomic architecture of the multivalent endemic black clam (Villorita cyprinoides) and its phylogenetic implications. Scientific Reports, 10(1): 15438, https://doi.org/10.1038/s41598-020-72194-1.
Ren J F, Liu X, Zhang G F et al. 2009. “Tandem duplication-random loss” is not a real feature of oyster mitochondrial genomes. BMC Genomics, 10(1): 84, https://doi.org/10.1186/1471-2164-10-84.
Ren J F, Shen X, Jiang F et al. 2010. The mitochondrial genomes of two scallops, Argopecten irradians and Chlamys farreri (Mollusca: Bivalvia): the most highly rearranged gene order in the family Pectinidae. Journal of Molecular Evolution, 70(1): 57–68, https://doi.org/10.1007/s00239-009-9308-4.
Ronquist F, Teslenko M, Van Der Mark P et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3): 539–542, https://doi.org/10.1093/sysbio/sys029.
Serb J M, Lydeard C. 2003. Complete mtDNA sequence of the North American freshwater mussel, Lampsilis ornata (Unionidae): an examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). Molecular Biology and Evolution, 20(11): 1854–1866, https://doi.org/10.1093/molbev/msg218.
Suchard M A, Lemey P, Baele G et al. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4(1): vey016, https://doi.org/10.1093/ve/vey016.
Sun S E, Jiang L S, Kong L F et al. 2020. Comparative mitogenomic analysis of the superfamily Tellinoidea (Mollusca: Bivalvia): insights into the evolution of the gene rearrangements. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 36: 100739, https://doi.org/10.1016/j.cbd.2020.100739.
Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56(4): 564–577, https://doi.org/10.1080/10635150701472164.
Taylor J D, Williams S T, Glover E A et al. 2007. A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S and 28S rRNA genes. Zoologica Scripta, 36(6): 587–606, https://doi.org/10.1111/j.1463-6409.2007.00299.x.
Van Damme D, Bogan A E, Dierick M. 2015. A revision of the Mesozoic naiads (Unionoida) of Africa and the biogeographic implications. Earth-Science Reviews, 147: 141–200, https://doi.org/10.1016/j.earscirev.2015.04.011.
Wang Y, Yang Y, Kong L F et al. 2023. Phylogenomic resolution of Imparidentia (Mollusca: Bivalvia) diversification through mitochondrial genomes. Marine Life Science & Technology, 5(3): 326–336, https://doi.org/10.1007/s42995-023-00178-x.
Wang Y, Yang Y, Liu H Y et al. 2021. Phylogeny of Veneridae (Bivalvia) based on mitochondrial genomes. Zoologica Scripta, 50(1): 58–70, https://doi.org/10.1111/zsc.12454.
Williams S T, Foster P G, Hughes C et al. 2017. Curious bivalves: systematic utility and unusual properties of anomalodesmatan mitochondrial genomes. Molecular Phylogenetics and Evolution, 110: 60–72, https://doi.org/10.1016/j.ympev.2017.03.004.
Wilson N G, Rouse G W, Giribet G. 2010. Assessing the molluscan hypothesis Serialia (Monoplacophora+Polyplacophora) using novel molecular data. Molecular Phylogenetics and Evolution, 54(1): 187–193, https://doi.org/10.1016/j.ympev.2009.07.028.
Wu X Y, Xu X D, Yu Z N et al. 2009. Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets. BMC Research Notes, 2: 69, https://doi.org/10.1186/1756-0500-2-69.
Xu X D, Wu X Y, Yu Z N. 2010. The mitogenome of Paphia euglypta (Bivalvia: Veneridae) and comparative mitogenomic analyses of three venerids. Genome, 53(12): 1041–1052, https://doi.org/10.1139/G10-096.
Xu X D, Wu X Y, Yu Z N. 2012. Comparative studies of the complete mitochondrial genomes of four Paphia clams and reconsideration of subgenus Neotapes (Bivalvia: Veneridae). Gene, 494(1): 17–23, https://doi.org/10.1016/j.gene.2011.12.002.
Yang M, Gong L, Sui J X et al. 2019. The complete mitochondrial genome of Calyptogena marissinica (Heterodonta: Veneroida: Vesicomyidae): insight into the deep-sea adaptive evolution of vesicomyids. PLoS One, 14(9): e0217952, https://doi.org/10.1371/journal.pone.0217952.
Zhang D, Gao F L, Jakovlic I et al. 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20(1): 348–355, https://doi.org/10.1111/1755-0998.13096.
Zieritz A, Froufe E, Bolotov I et al. 2021. Mitogenomic phylogeny and fossil-calibrated mutation rates for all F-and M-type mtDNA genes of the largest freshwater mussel family, the Unionidae (Bivalvia). Zoological Journal of the Linnean Society, 193(3): 1088–1107, https://doi.org/10.1093/zoolinnean/zlaa153.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Supported by the Research and Development Program of Shandong Province, China (Major Science and Technology Innovation Project) (No. 2021CXGC011306), the MNR Key Laboratory of Eco-Environmental Science and Technology, China (No. MEEST-2021-05), the Natural Science Foundation of Shandong Province (No. ZR2020MD002), the Doctoral Science Research Foundation of Yantai University (Nos. SM15B01, SM19B70, SM19B28), and the “Double-Hundred Action” of Yantai City (No. 2320004-SM20RC02)
Rights and permissions
About this article
Cite this article
Wang, X., Zhang, H., Teng, X. et al. Mitochondrial genomes of Tapes dorsatus and Cardita variegata: insights into Heteroconchia phylogeny. J. Ocean. Limnol. 42, 943–959 (2024). https://doi.org/10.1007/s00343-023-3059-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-023-3059-8