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Characterization of the complete mitochondrial genome of the brazilian cownose ray Rhinoptera brasiliensis (Myliobatiformes, Rhinopteridae) in the western Atlantic and its phylogenetic implications

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Abstract

Background

The Brazilian cownose ray, Rhinoptera brasiliensis has undergone a global population reduction and is currently classified by IUCN as Vulnerable. This species is sometimes confused with Rhinoptera bonasus, the only external diagnostic characteristic to distinguish between both species is the number of rows of tooth plates. Both cownose rays overlap geographically from Rio de Janeiro to the western North Atlantic. This calls for a more comprehensive phylogenetic assessment using mitochondria DNA genomes to better understand the relationships and delimitation of these two species.

Methods and results

The mitochondrial genome sequences of R. brasiliensis was obtained by next-generation sequencing. The length of the mitochondrial genome was 17,759 bp containing 13 protein-coding genes (PCGs), two ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, and a non-coding control region (D-loop). Each PCG was initiated by an authoritative ATG codon, except for COX1 initiated by a GTG codon. Most of the PCGs were terminated by a complete codon (TAA/TAG), while an incomplete termination codon (TA/T) was found in five out of the 13 PCGs. The phylogenetic analysis showed that R. brasiliensis was closely related to R. steindachneri whereas the reported mitogenome as R. steindachneri (GenBank accession number KM364982), differs from multiple mitocondrial DNA sequences of R. steindachneri and is nearly identical to that of R. javanica.

Conclusion

The new mitogenome determined in this study provides new insight into the phylogenetic relationships in Rhinoptera, while providing new molecular data that can be applied to population genetic studies.

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References

  1. Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138. https://doi.org/10.1016/S1055-7903(02)00332-9

    Article  CAS  PubMed  Google Scholar 

  2. Inoue JG, Kumazawa Y, Miya M, Nishida M (2009) The historical biogeography of the freshwater knifefishes using mitogenomic approaches: a mesozoic origin of the asian notopterids (Actinopterygii: Osteoglossomorpha). Mol Phylogenet Evol 51(3):486–499. https://doi.org/10.1016/j.ympev.2009.01.020

    Article  CAS  PubMed  Google Scholar 

  3. Galtier N, Nabholz B, Glemin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550

    Article  CAS  PubMed  Google Scholar 

  4. Poortvliet M, Olsen JL, Croll DA, Bernardi G, Newton K, Kollias S, O’Sullivan J, Fernando D, Stevens G, Galván-Magaña F, Seret B, Wintner S, Hoarau G (2015) A dated molecular phylogeny of manta and devil rays (Mobulidae) based on mitogenome and nuclear sequences. Mol Phylogenet Evol 83:72–85. https://doi.org/10.1016/j.ympev.2014.10.012

    Article  CAS  PubMed  Google Scholar 

  5. Martin AP, Naylor GJ, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155

    Article  CAS  PubMed  Google Scholar 

  6. Martin AP (1995) Mitochondrial DNA sequence evolution in sharks: rates, patterns, and phylogenetic inferences. Mol Biol Evol 12:1114–1123

    CAS  PubMed  Google Scholar 

  7. Stepien CA, Kocher TD (1997) Molecules and morphology in studies of Fish Evolution. Molecular Systematics of Fishes. Elsevier, New York, NY, USA, pp 1–11

    Google Scholar 

  8. Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular phylogenetics: a tree-based exploration under the maximum parsimony optimality criterion. Mol Phylogenet Evol 17:437–455

    Article  CAS  PubMed  Google Scholar 

  9. Alam MT, Petit RA, Read TD, Dove ADM (2014) The complete mitochondrial genome sequence of the world’s largest fish, the whale shark (Rhincodon typus), and its comparison with those of related shark species. Gene 539:44–49

    Article  CAS  PubMed  Google Scholar 

  10. Gillett CPDT, Crampton-Platt A, Timmermans MJTN, Jordal BH, Emerson BC, Vogler AP (2014) Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea). Mol Biol Evol 31:2223–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kousteni V, Mazzoleni S, Vasileiadou K, Rovatsos M (2021) Complete mitochondrial DNA genome of nine species of sharks and rays and their phylogenetic placement among modern Elasmobranchs. Genes 12:324. https://doi.org/10.3390/genes12030324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Last PR, White W, de Carvalho MR, Séret B, Stehmann M, Naylor G (2016) Rays of the world. CSIRO Publishing, Clayton North, p 790

    Book  Google Scholar 

  13. Fisher RA, Call GC, McDowell JR (2014) Reproductive variations in Cownose Rays (Rhinoptera bonasus) from Chesapeake Bay. Environ Biol Fish 97:1031–1038

    Article  Google Scholar 

  14. Poulakis GR (2013) Reproductive biology of the Cownose Ray in the Charlotte Harbor estuarine system, Florida. Mar Coastal Fisheries 5:159–173

    Article  Google Scholar 

  15. Menni RC, Stehmann MFW (2000) Distribution, environment and biology of batoid fishes of Argentina, Uruguay and Brazil, a review. Revista del Museo Argentino de Ciencias Naturales Nueva Serie 2:69–109. https://doi.org/10.22179/REVMACN.2.126

    Article  Google Scholar 

  16. Barker AS (2006) Rhinoptera bonasus. The IUCN Red List of Threatened Species 2006: e.T60128A12310195. Available from: http://www.iucnredlist.org/details/60128/0

  17. Palacios-Barreto P, Cruz VP, Foresti F, Rangel BS, Uribe-Alcocer M, Díaz-Jaimes P (2017) Molecular evidence supporting the expansion of the geographical distribution of the Brazilian cownose ray Rhinoptera brasiliensis (Myliobatiformes: Rhinopteridae) in the western Atlantic. Zootaxa, 4341, 593–600. https://doi.org/10.11646/Zootaxa.4341.4.12. PMID: 29245683

  18. Jones CM, Hoffmayer ER, Hendon JM, Quattro JM, Lewandowski J, Roberts MA, Márquez-Farías JF (2017) Morphological conservation of rays in the genus Rhinoptera (Elasmobranchii, Rhinopteridae) conceals the occurrence of a large batoid, Rhinoptera brasiliensis Müller, in the northern Gulf of Mexico. Zootaxa 4286:499–514

    Article  Google Scholar 

  19. Weber HK, Jones CM, Ajemian MJ, McCallister MP, Winner BL, Poulakis GR, Bethea DM, Hollensead LD, Zapf D, Swenson JD, Hendon JM, Daly-Engel TS, Phillips NM (2021) Genetic evidence supports a range extension for the brazilian cownose ray Rhinoptera brasiliensis in the western North Atlantic. J Fish Biol 98:577–582. https://doi.org/10.1111/jfb.14582

    Article  CAS  PubMed  Google Scholar 

  20. White WT, Corrigan S, Yang L, Henderson AC, Bazinet AL, Swofford DL, Naylor GJP (2018) Phylogeny of the manta and devilrays (Chondrichthyes: Mobulidae), with an updated taxonomic arrangement for the family. Zool J Linn Soc 182(1):50–75. https://doi.org/10.1093/zoolinnean/zlx018

    Article  Google Scholar 

  21. Aschliman NC, Nishida M, Miya M, Inoue JG, Rosana KM, Naylor GJ (2012) Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Mol Phylogenet Evol Apr 63(1):28–42. https://doi.org/10.1016/j.ympev.2011.12.012

    Article  Google Scholar 

  22. McEachran JD, de Carvalho MR (2002) Batoid fishes. In: Carpenter KE (ed) The living marine resources of the western Central Atlantic. Vol. 1. Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes and chimaeras, vol 5. FAO Species Identification Guide for Fisheries Purposes and American Society of Ichthyologists and Herpetologists Special Publication, pp 508–530

  23. Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez NJ, Finger JW, Pierson TW, Bentley KE, Hoffberg SL, Louha S, Garcia-De Leon FJ, Del Rio Portilla MA, Reed KD, Anderson JL, Meece JK, Aggrey SE, Rekaya R, Alabady M, Belanger M, Winker K, Faircloth BC (2019) Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ 7:e7755. https://doi.org/10.7717/peerj.7755

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22(5):939–946. https://doi.org/10.1101/gr.128124.111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Andrews S (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  26. Hahn C, Bachmann L, Chevreux B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads – a baiting and iterative mapping approach. Nucleic Acids Res 41:e129. https://doi.org/10.1093/nar/gkt371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, Sado T, Mabuchi K, Takeshima H, Miya M, Nishida M (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biology Evol 30:2531–2540. https://doi.org/10.1093/molbev/mst141

    Article  CAS  Google Scholar 

  28. Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol Jun 25(7):3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  Google Scholar 

  29. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–335. https://doi.org/10.1007/BF00186547

    Article  CAS  PubMed  Google Scholar 

  30. Lowe TM, Chan PP (2016) tRNAscan-SE On-line: search and contextual analysis of transfer RNA genes. Nucl Acids Res 44:W54–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69(2):313–319. https://doi.org/10.1016/j.ympev.2012.08.023

    Article  PubMed  Google Scholar 

  32. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580. https://doi.org/10.1093/nar/27.2.573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–971792. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large Model Space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  37. Kimura M (1980) A simple method of estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  38. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  PubMed  Google Scholar 

  39. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2:e312. https://doi.org/10.1371/JOURNAL.PBIO.0020312

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vella N, Vella A (2021) Characterization and comparison of the complete mitochondrial genomes of two stingrays, Dasyatis pastinaca and Dasyatis tortonesei (Myliobatiformes: Dasyatidae) from the Mediterranean Sea. Mol Biol Rep 48(1):219–226. https://doi.org/10.1007/s11033-020-06038-6

    Article  CAS  PubMed  Google Scholar 

  41. Wang IC, Lin HD, Liang CM, Huang CC, Wang RD, Yang JQ, Wang WK (2020) Complete mitochondrial genome of the freshwater fish Onychostoma lepturum (Teleostei, Cyprinidae): genome characterization and phylogenetic analysis. ZooKeys 1005:57–72. https://doi.org/10.3897/zookeys.1005.57592

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sun CH, Liu HY, Xu N, Zhang XL, Zhang Q, Han BP (2021) Mitochondrial genome structures and phylogenetic analyses of two tropical Characidae fishes. Front Genet 12:e627402. https://doi.org/10.3389/fgene.2021.627402

    Article  CAS  Google Scholar 

  43. Zhang J, Yang B, Yamaguchi A, Furumitsu K, Zhang B (2015) Mitochondrial genome of longheaded eagle ray Aetobatus flagellum (Chondrichthyes: Myliobatidae). Mitochondrial DNA 26(5):763–764. https://doi.org/10.3109/19401736.2013.855740

    Article  CAS  PubMed  Google Scholar 

  44. Li R, Lei Z, Li W, Zhang W, Zhou C (2021) Comparative mitogenomics analysis of Heptageniid Myflies (Insecta: Ephemeroptera): conserved intergenic spacer and tRNA gene duplication. Insects 12:170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Díaz-Jaimes P, Bayona-Vásquez NJ, Adams DH, Uribe-Alcocer M (2016) Complete mitochondrial DNA genome of bonnethead shark, Sphyrna tiburo, and phylogenetic relationships among main superorders of modern elasmobranchs. Meta Gene 7:48–55

    Article  PubMed  Google Scholar 

  46. Sangster G, Luksenburg JA (2021) The published complete mitochondrial genome of the milk shark (Rhizoprionodon acutus) is a misidentified Pacific spadenose shark (Scoliodon macrorhynchos) (Chondrichthyes: Carcharhiniformes). Mitochondrial DNA Part B 6(3):828–830. https://doi.org/10.1080/23802359.2021.1884019

    Article  PubMed  PubMed Central  Google Scholar 

  47. Nwobodo AK, Li M, An L, Cui M, Wang C, Wang A, Chen Y, Du S, Feng C, Zhong S, Gao Y, Cao X, Wang L, Obinna EM, Mei X, Song Y, Li Z, Qi D (2019) Comparative analysis of the complete mitochondrial genomes for Development Application. Front Genet 9:1–12

    Google Scholar 

  48. Chen X, Sonchaeng P, Yuvanatemiya V, Nuangsaeng B, Ai W (2016) Complete mitochondrial genome of the withetip reef shark Triaenodon obesus (Carcharhiniformes: Carcharhinidae). Mitochondrial DNA Part A 27:947–948

    Article  Google Scholar 

  49. Zhu K-C, Liang Y-Y, Wu N, Guo H-Y, Zhang N, Jiang S-G, Zhang D-C (2017) Sequencing and characterization of the complete mitochondrial genome of Japanise Swellshark (Cephalloscyllium umbratile). Sci Rep 7:e15299. https://doi.org/10.1038/s41598-017-15702-0

    Article  CAS  Google Scholar 

  50. Mar-Silva AF, Díaz-Jaimes P, Arroyave J (2022) The complete mitocondrial genome of the mexican-endemic cavefish Ophisternon infernale (Synbranchiformes, Synbranchidae): insights on patterns of selection and implications for synbranchiform phylogenetics. ZooKeys 1089:1–23

    Article  PubMed  PubMed Central  Google Scholar 

  51. Naylor GJP, Caira JN, Jensen K, Rosana KAM, Straube N, Lakner C (2012) Elasmobranch phylogeny: A mitochondrial estimate based on 595 species. In Biology of Sharks and Their Relatives, 2nd ed.; Carrier JC, Musick JA, Heithaus MR Eds. CRC Press: Boca Raton, FL, USA, 2012; pp. 31–56

  52. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857. https://doi.org/10.1098/RSTB.2005.1716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The first author acknowledges the Posgrado en Ciencias del Mar y Limnología, and CONACYT for Ph.D. for providing the necessary facilities for conducting the research. Company Bioinformatic analyses were carried out on HP system cluster platform 3000SL “Miztli” under Project LANCAD-UNAM-DGTIC-341. The authors thanks editor and anonymous reviewers for their suggestions to improve the manuscript quality. Authors are grateful to the two reviewers who improved notably the manuscript.

Funding

This study was supported by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT), UNAM (Grant number IN207621). Author P.P.B. has received research support from CONACYT and PAPIIT.

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Authors and Affiliations

  1. Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria 3000, C.P. 04510, Coyoacán, Ciudad de México, México

    Paola Palacios-Barreto & Adán Fernando Mar-Silva

  2. Fundación colombiana para la investigación y conservación de Tiburones y Rayas, SQUALUS, Cali, Colombia

    Paola Palacios-Barreto

  3. Division of Natural Science and Mathematics, Oxford College, Emory University, 30054, Oxford, GA, USA

    Natalia J. Bayona-Vasquez

  4. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Indian River Field Laboratory, 32901, Melbourne, FL, USA

    Douglas H. Adams

  5. Unidad Académica de Ecología y Biodiversidad Acuática, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad de México, México

    Píndaro Díaz-Jaimes

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  1. Paola Palacios-Barreto
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  2. Adán Fernando Mar-Silva
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  5. Píndaro Díaz-Jaimes
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Contributions

All authors contributed to the study conception and design. PPB: Material preparation, collected the sample, Methodology, Writing—Original Draft, Data Curation & Editing, AFMS: Methodology & formal analysis, NJBV: Data Curation &Writing—Review, DHA: Supervision, Writing—Review & Editing PDJ: Supervision, Writing—Review & Editing, and All authors read and approved the final manuscript.

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Correspondence to Píndaro Díaz-Jaimes.

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This study did not require ethical approval as it made use of muscle tissue collected from dead specimens that were caught by local fishers and were to be sold at the respective local fish markets.

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Palacios-Barreto, P., Mar-Silva, A.F., Bayona-Vasquez, N.J. et al. Characterization of the complete mitochondrial genome of the brazilian cownose ray Rhinoptera brasiliensis (Myliobatiformes, Rhinopteridae) in the western Atlantic and its phylogenetic implications. Mol Biol Rep 50, 4083–4095 (2023). https://doi.org/10.1007/s11033-023-08272-0

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