Amplicon sequencing reveals the cryptic diversity in the dicyemid parasites of coleoid cephalopods sampled from the Atlantic and Pacific Oceans

Tijana Cvetković , Masoud Nazarizadeh , Tereza Koudelková , Fedor Lishchenko , Yen H. T. Dinh , Eduardo Almansa , Hannah Osland , Tomáš Scholz , Zdeněk Lajbner , Qiaz Q. H. Hua , Marie Drábková , Jan Štefka

Marine Life Science & Technology ›› : 1 -16.

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Marine Life Science & Technology ›› :1 -16. DOI: 10.1007/s42995-026-00353-w
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Amplicon sequencing reveals the cryptic diversity in the dicyemid parasites of coleoid cephalopods sampled from the Atlantic and Pacific Oceans

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Abstract

Dicyemids (phylum Dicyemida), primarily found in the renal organs of coleoid cephalopods, are a unique group of morphologically simple parasites with global distribution. Here, we investigated the diversity and prevalence of dicyemid communities in a wide range of cephalopod hosts across four geographic zones (the North East Atlantic, Mediterranean Sea, China Sea in the Western North Pacific, and Australia in the South Pacific) using Illumina sequencing of the 18S rDNA amplicons. Across 227 host samples, we identified 482 amplicon sequence variants, which clustered into 95 genetic types. The results indicated a higher number of distinct genetic types within Dicyemida than those currently identified through morphology-based taxonomy. Our finding of 46 dicyemid types in the common cuttlefish (Sepia officinalis) contrasts sharply with the previous records of a maximum of four species in this host. Furthermore, only a few host species exhibited a single dicyemid type, while most harbored multiple types; several types were distributed worldwide. Additionally, we identified eight new cephalopod hosts in the Pacific. Analyses of community (α) diversity suggested the unique character of certain geographical areas, such as the Bass Strait (Australia). β-diversity analyses confirmed that geographic location and host species were significant determinants of the dicyemid community composition. These results suggest that current species classifications may underestimate the true diversity of dicyemids. They emphasize the intricate interplay between geography, host specificity, and dicyemid community diversity.

Keywords

Dicyemida / Cephalopods / Host–parasite assemblage / Amplicon sequencing / Biodiversity

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Tijana Cvetković, Masoud Nazarizadeh, Tereza Koudelková, Fedor Lishchenko, Yen H. T. Dinh, Eduardo Almansa, Hannah Osland, Tomáš Scholz, Zdeněk Lajbner, Qiaz Q. H. Hua, Marie Drábková, Jan Štefka. Amplicon sequencing reveals the cryptic diversity in the dicyemid parasites of coleoid cephalopods sampled from the Atlantic and Pacific Oceans. Marine Life Science & Technology 1-16 DOI:10.1007/s42995-026-00353-w

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References

[1]

Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Xu ZZ, Kightley EP, Thompson LR, Hyde ER, Gonzalez A, Knight R. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems, 2017, 2: e00191-16

[2]

Anderson MJ. Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef statistics reference online, 2017, Hoboken, NJ, John Wiley & Sons Ltd1-15

[3]

Anderson MJ, Walsh DC. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing?. Ecol Monogr, 2013, 83: 557-574

[4]

Andrews S (2010) FastQC: a quality control tool for high-throughput sequence data. Accessed December 2022.

[5]

Aruga J, Odaka YS, Kamiya A, Furuya H. Dicyema Pax6 and Zic: toolkit genes in a highly simplified bilaterian. BMC Evol Biol, 2007, 7: 201

[6]

Awata H, Noto T, Endoh H. Differentiation of somatic mitochondria and the structural changes in mtDNA during development of the dicyemid Dicyema japonicum (Mesozoa). Mol Genet Genomics, 2006, 273: 441-449

[7]

Bleidorn C. Recent progress in reconstructing lophotrochozoan (Spiralian) phylogeny. Org Divers Evol, 2019, 19: 557-566

[8]

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EKet al.. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37: 852-857

[9]

Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MAet al.. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol, 2019, 15: e1006650

[10]

Bouzid W, Štefka J, Hypša V, Lek S, Scholz T, Legal L, Hassine OKB, Loot G. Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int J Parasitol, 2008, 38: 1465-1479

[11]

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods, 2016, 13: 581-583

[12]

Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME, 2017, 11: 2639-2643

[13]

Castellanos-Martinez S, Gómez MC, Hochberg FG, Gestal C, Furuya H. A new dicyemid from Octopus hubbsorum (Mollusca: Cephalopoda: Octopoda). J Parasitol, 2011, 97: 265-269

[14]

Castellanos-Martinez S, Aguirre-Macedo ML, Furuya H. Two new species of dicyemid mesozoans (Dicyemida: Dicyemidae) from Octopus maya Voss & Solis-Ramirez (Octopodidae) off Yucatan, Mexico. Syst Parasitol, 2016, 93: 551-564

[15]

Catalano SR. A review of the families, genera, and species of Dicyemida van Beneden, 1876. Zootaxa, 2012, 3479: 1-32

[16]

Catalano SR. Five new species of dicyemid mesozoans (Dicyemida: Dicyemidae) from two Australian cuttlefish species, with comments on dicyemid fauna composition. Syst Parasitol, 2013, 86: 125-151

[17]

Catalano SR. First descriptions of dicyemid mesozoans (Dicyemida: Dicyemidae) from Australian octopus (Octopodidae) and cuttlefish (Sepiidae) species, including a new record of Dicyemennea in Australian waters. Folia Parasitol, 2013, 60: 306-320

[18]

Catalano SR, Furuya H. Two new species of dicyemid (Dicyemida: Dicyemidae) from two Australian cephalopod species: Sepioteuthis australis (Mollusca: Cephalopoda: Loliginidae) and Sepioloidea lineolata (Mollusca: Cephalopoda: Sepiadariidae). J Parasitol, 2013, 99: 203-211

[19]

Catalano SR, Whittington ID, Donnellan SC, Gillanders BM. Using the giant Australian cuttlefish (Sepia apama) mass breeding aggregation to explore the life cycle of dicyemid parasites. Acta Parasitol, 2013, 58: 229-238

[20]

Catalano SR, Whittington ID, Donnellan SC, Gillanders BM. Dicyemid fauna composition and infection patterns in relation to cephalopod host biology and ecology. Folia Parasitol, 2014, 61: 301-310

[21]

Chaudhry U, Ali Q, Rashid I, Shabbir MZ, Ijaz M, Abbas M, Evans M, Ashraf K, Morrison I, Morrison L, Sargison ND. Development of a deep amplicon sequencing method to determine the species composition of piroplasm haemoprotozoa. Ticks Tick Borne Dis, 2019, 10: 101276

[22]

Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol, 1993, 18: 117-143

[23]

Combes C. Parasitism: the ecology and evolution of intimate interactions, 2001, Chicago, University of Chicago Press

[24]

Drábková M, Jachníková N, Tyml T, Sehadová H, Ditrich O, Myšková E, Hypša V, Štefka J. Population co-divergence in common cuttlefish (Sepia officinalis) and its dicyemid parasite in the Mediterranean Sea. Sci Rep, 2019, 9: 50555

[25]

Drábková M, Flegrová T, Myšková E, Hypša V, Štefka J. Genetic analysis of dicyemid infrapopulations suggests sexual reproduction and host colonization by multiple individuals is common. Org Divers Evol, 2021, 21: 437-446

[26]

Drábková M, Kocot KM, Halanych KM, Oakley TH, Moroz LL, Cannon JT, Kuris A, Garcia-Vedrenne AE, Pankey MS, Ellis EA, Varney R, Štefka J, Zrzavý J. Different phylogenomic methods support monophyly of enigmatic ‘Mesozoa’ (Dicyemida + Orthonectida, Lophotrochozoa). Proc R Soc Lond B Biol Sci, 2022, 289: 20220683

[27]

Dunn CW, Giribet G, Edgecombe GD, Hejnol A. Animal phylogeny and its evolutionary implications. Annu Rev Ecol Evol Syst, 2014, 45: 371-395

[28]

Edgar RC. UNOISE2 improved error correction for Illumina 16S and its amplicon sequencing. bioRxiv, 2016

[29]

Erdl. Ueber die beweglichen Faden in den Venenanhangen der Cephalopoden. Archiv Für Naturgeschichte, 1843, 1: 162-167

[30]

Eren AM, Maignien L, Sul WJ, Murphy LG, Grim SL, Morrison HG, Sogin ML. Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol Evol, 2013, 4: 1111-1119

[31]

Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME, 2015, 9: 968-979

[32]

Eshragh R, Leander BS. Molecular contributions to species boundaries in dicyemid parasites from eastern Pacific cephalopods. Mar Biol Res, 2014, 11: 414-422

[33]

Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinform, 2016, 32: 3047-3048

[34]

Ezard T, Fujisawa T, Barraclough TG (2009) SPLITS: SPecies’ LImits by Threshold Statistics. R package version 1.0–20/r45. Available from: https://r-forge.r-project.org/projects/splits/. Accessed February 2022.

[35]

Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv, 1992, 61: 1-10

[36]

Finn JK, Hochberg FG, Norman MD. Phylum dicyemida in Australian waters: first record and distribution across diverse cephalopod hosts. Phuket Mar Biol Cent Res Bull, 2005, 66: 83-96

[37]

Frishkoff LO, Karp DS, M’Gonigle LK, Hadly EA, Daily GC, Mendenhall CD. Loss of avian phylogenetic diversity in neotropical agricultural systems. Science, 2014, 345: 1343-1346

[38]

Furuya H. Fourteen new species of dicyemid mesozoans from six Japanese cephalopods, with comments on host specificity. Species Divers, 1999, 4: 257-319

[39]

Furuya H. Motokawa M, Kajihara H. Diversity and morphological adaptation of dicyemids in Japan. Species diversity of animals in Japan, 2016, Tokyo, Springer Japan401418

[40]

Furuya H. Eleven new species of dicyemids (phylum Dicyemida) from Octopus longispadiceus and O. tenuicirrus (Mollusca: Cephalopoda: Octopoda) in Japanese waters. Species Divers, 2018, 23: 143-179

[41]

Furuya H, Moritaki T. Fourteen new species of dicyemids (Phylum: Dicyemida) from seven species of Decapodiformes (Mollusca: Cephalopoda) in the Kumano Sea, Japan. Species Divers, 2022, 27: 181-226

[42]

Furuya H, Souidenne D. Gestal C, Pascual S, Guerra Á, Fiorito G, Vieites J. Dicyemids. Handbook of pathogens and diseases in cephalopods, 2019, Cham, Springer179199

[43]

Furuya H, Tsuneki K. Biology of dicyemid mesozoans. Zool Sci, 2003, 20: 519-532

[44]

Furuya H, Tsuneki K. A new species of dicyemid mesozoan (Dicyemida: Dicyemidae) from Sepioteuthis lessoniana (Mollusca: Cephalopoda), with notes on Dicyema orientale. Species Divers, 2005, 10: 45-62

[45]

Furuya H, Hochberg FG, Tsuneki K. Calotte morphology in the phylum Dicyemida: niche separation and convergence. J Zool, 2003, 259: 361-373

[46]

Furuya H, Ota M, Kimura R, Tsuneki K. Renal organs of cephalopods: a habitat for dicyemids and chromidinids. J Morphol, 2004, 262: 629-643

[47]

Gestal C, Abollo E, Arias C, Pascual S. Dicyema typus Van Beneden, 1876 (Mesozoa: Dicyemidae), a "kidney" mesozoan parasite of Octopus vulgaris Cuvier, 1797 (Mollusca: Cephalopoda) from NW Spain. Res Rev Parasitol, 1997, 57: 85-87

[48]

Hammoud C, Mulero S, Van Bocxlaer B, Boissier J, Verschuren D, Albrecht C, Huyse T. Simultaneous genotyping of snails and infecting trematode parasites using high‐throughput amplicon sequencing. Mol Ecol Resour, 2021, 22: 567-586

[49]

Hochberg FG. Kinne O. Diseases of Mollusca: Cephalopoda: diseases caused by protistans and metazoans. Diseases of marine animals, 1990, Hamburg, Biologisches Anstalt Helgoland47227III

[50]

Hudson PJ, Rizzoli A, Grenfell BT, Heersterbeek H, Dobson AP. The ecology of wildlife diseases, 2002, Oxford, Oxford University Press

[51]

Johnson P, Thieltges DW. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol, 2010, 213: 961-970

[52]

Kopylova E, Navas-Molina JA, Mercier C, Xu ZZ, Mahé F, He Y, Zhou HW, Rognes T, Caporaso JG, Knight R. Open-source sequence clustering methods improve the state of the art. mSystems, 2016, 1: e00003-15

[53]

Krohn A. Ueber das Vorkommen von Entozoën und Kristallablagerungen in den schwammigen Venenanhängen einiger Cephalopoden. Froriep’s Neue Notizen, 1839, 11: 213-216

[54]

Lajeunesse MJ, Forbes MR. Host range and local parasite adaptation. Proc Biol Sci, 2002, 269: 703-710

[55]

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol, 2017, 34: 772-773

[56]

Lapan EA, Morowitz HJ. The dicyemid mesozoa as an integrated system for morphogenetic studies. I. Description, isolation, and maintenance. J Exp Zool, 1975, 193: 147-159

[57]

Lu TM, Kanda M, Satoh N, Furuya H. The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution. Zool Lett, 2017, 3: 6

[58]

Lu TM, Kanda M, Furuya H, Satoh N. Dicyemid mesozoans: a unique parasitic lifestyle and a reduced genome. Genome Biol Evol, 2019, 11: 2232-2243

[59]

MacConaill LE, Burns RT, Nag A, Coleman HA, Slevin MK, Giorda K, Light M, Lai K, Jarosz M, McNeill MS, Ducar MD, Meyerson M, Thorner AR. Unique, dual-indexed sequencing adapters with UMIs effectively eliminate index cross-talk and significantly improve sensitivity of massively parallel sequencing. BMC Genomics, 2018, 19: 30

[60]

McConnaughey BH. The life cycle of the dicyemid mesozoa. Univ Calif Publ Zool, 1951, 55: 295-336

[61]

Nakajima H, Fukui A, Suzuki K, Kharisma Tirta TY, Furuya H. Host switching in dicyemids (Phylum Dicyemida). J Parasitol, 2024, 110: 159-169

[62]

Nazarizadeh M, Nováková M, Loot G, Gabagambi NP, Fatemizadeh F, Osano O, Presswell B, Poulin R, Vitál Z, Scholz T, Halajian A, Trucchi E, Kočová P, Štefka J. Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite—the Ligula intestinalis species complex. Mol Phylogenet Evol, 2023, 180: 107677

[63]

Nouvel H. Les Dicyemides. 1re partie: systématique, générations vermiformes, infusorigène et sexualité. Arch Biol, 1947, 58: 59-220

[64]

Ogedengbe JD, Hanner RH, Barta JR. DNA barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). Int J Parasitol, 2011, 41: 843-850

[65]

Palumbi SR. Marine speciation on a small planet. Trends Ecol Evol, 1992, 7: 114-118

[66]

Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol, 2006, 55: 595-609

[67]

Poulin R. Evolutionary ecology of parasites (Second Edition), 2007Princeton University Press

[68]

Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol, 2009, 26: 1641-1650

[69]

R Core Team. R: a language and environment for statistical computing, 2021, Vienna, Austria, R Foundation for Statistical Computing

[70]

Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol, 2018, 67: 901-904

[71]

Reid NM, Carstens BC. Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol, 2012, 12: 196

[72]

Reid NM, Hird SM, Brown JM, Pelletier TA, McVay JD, Satler JD, Carstens BC. Poor fit to the multispecies coalescent is widely detectable in empirical data. Syst Biol, 2013, 63: 322-333

[73]

Rich RL, Mueller P, Fuß M, Gonçalves S, Ostertag E, Reents S, Tang H, Tashjian A, Thomsen S, Kutzbach L, Jensen K, Nolte S. Design and assessment of a novel approach for ecosystem warming experiments in high-energy tidal wetlands. J Geophys Res Biogeosci, 2023, 128: e2023JG007550

[74]

Roper CF, Sweeney MJ, Nauen C (1984) Cephalopods of the world: an annotated and illustrated catalogue of species of interest to fisheries. FAO Species Catalogue Vol. 3.

[75]

Roumbedakis K, Drábková M, Tyml T, di Cristo C. A perspective around cephalopods and their parasites, and suggestions on how to increase knowledge in the field. Front Physiol, 2018, 9: 1573

[76]

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol, 2017, 34: 3299-3302

[77]

RStudio Team. RStudio: integrated development for R, 2020, PBC, Boston, MA, RStudio

[78]

Schiffer PH, Robertson HE, Telford MJ. Orthonectids are highly degenerate annelid worms. Curr Biol, 2018, 28: 1971-1977

[79]

Schmidt TSB, Matias Rodrigues JF, von Mering C. Ecological consistency of SSU rRNA-based operational taxonomic units at a global scale. PLoS Comput Biol, 2014, 10: e1003594

[80]

Sharda M (2020) MetReTrim: this pipeline trims heterogeneity ‘n’ spacers from the pre-processed reads given the primer sequences. GitHub Repository. Available at: https://github.com/Mohak91/MetReTrim. Accessed July 10, 2021.

[81]

Souidenne D, Florent I, Dellinger M, Romdhane MS, Grellier P, Furuya H. Redescription of Dicyemennea eledones (Wagener, 1857) (Phylum Dicyemida) from Eledone cirrhosa (Lamarck, 1798) (Mollusca: Cephalopoda: Octopoda). Syst Parasitol, 2016, 93: 905-915

[82]

Stevenson M, Stevenson MM, BiasedUrn I (2015) Package ‘epiR’: tools for the analysis of epidemiological data. R package version 0.9–62. Available at: https://cran.r-project.org/web/packages/epiR/

[83]

Stunkard HW. The life-history and systematic relations of the Mesozoa. Q Rev Biol, 1954, 29: 230-244

[84]

Suzuki TG, Ogino K, Tsuneki K, Furuya H. Phylogenetic analysis of dicyemid mesozoans (phylum Dicyemida) from innexin amino acid sequences: dicyemids are not related to Platyhelminthes. J Parasitol, 2010, 96: 614-625

[85]

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol, 2013, 30: 2725-2729

[86]

Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG, Fontaneto D. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc Natl Acad Sci USA, 2012, 109: 16208-16212

[87]

Tedesco P, Bevilacqua S, Fiorito G, Terlizzi A. Global patterns of parasite diversity in cephalopods. Sci Rep, 2020, 10: 11303

[88]

Telford MJ, Budd GE, Philippe H. Phylogenomic insights into animal evolution. Curr Biol, 2015, 25: R876-R887

[89]

Thompson JN. The geographic mosaic of coevolution (interspecific interactions), 2005, Chicago, IL, University of Chicago Press400

[90]

Tikhonov M, Leach RW, Wingreen NS. Interpreting 16S metagenomic data without clustering to achieve sub-OTU resolution. ISME J, 2015, 9: 68-80

[91]

Van Beneden E. Recherches sur les Dicyemides, survivants actuels d’un embranchement des Mesozoaires. Bull Acad R Belg, 1876, 41: 1160-1205

[92]

Van Beneden E. Contribution à l’histoire des Dicyemides. Arch Biol, 1882, 3: 197-228

[93]

Von Kölliker A. Ueber Dicyema paradoxum, den Schmarotzer der Venenanhänge der Cephalopoden. Berichte Von der Königlichen Zootomischen Anstalt Zu Wurzburg., 1849, 2: 53-58

[94]

Westcott SL, Schloss PD. De novo clustering methods outperform reference-based methods for assigning 16S rRNA gene sequences to operational taxonomic units. PeerJ, 2015, 3: e1487

[95]

Whiteman NK, Parker PG. Effects of host sociality on ectoparasite population biology. J Parasitol, 2004, 90: 939-947

[96]

Whittaker RH. Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr, 1960, 30: 279-338

[97]

Xia X. DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Mol Biol Evol, 2018, 35: 1550-1552

[98]

Xia X, Xie Z, Salemi M, Chen L, Wang Y. An index of substitution saturation and its application. Mol Phylogenet Evol, 2003, 26: 1-7

[99]

Zhang J, Kapli P, Pavlidis P, Stamatakis A. A general species delimitation method with applications to phylogenetic placements. Bioinform, 2013, 29: 2869-2876

[100]

Zheng X, Ikeda M, Kong L, Lin X, Li Q, Taniguchi N. Genetic diversity and population structure of the golden cuttlefish, Sepia esculenta (Cephalopoda: Sepiidae) indicated by microsatellite DNA variations. Mar Ecol, 2009, 30: 448-454

[101]

Zheng JJ, Wang PW, Huang TW, Yang YJ, Chiu HS, Sumazin P, Chen TW. MOCHI: a comprehensive cross-platform tool for amplicon-based microbiota analysis. Bioinform, 2022, 38: 4286-4292

[102]

Zrzavý J. The interrelationships of metazoan parasites: a review of phylum- and higher-level hypotheses from recent morphological and molecular phylogenetic analyses. Folia Parasitol, 2001, 48: 81-103

[103]

Zverkov OA, Mikhailov KV, Isaev SV, Rusin LY, Popova OV, Logacheva MD, Penin AA, Moroz LL, Panchin YV, Lyubetsky VA, Aleoshin VV. Dicyemida and orthonectida: two stories of body plan simplification. Front Genet, 2019, 10: 443

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