Hostname: page-component-7479d7b7d-c9gpj Total loading time: 0 Render date: 2024-07-12T01:52:30.028Z Has data issue: false hasContentIssue false

Species identification and genetic relationships in the squid family Gonatidae (Teuthida, Cephalopoda) based on partial sequencing of mitochondrial and nuclear genes

Published online by Cambridge University Press:  03 November 2023

Oleg N. Katugin
Affiliation:
Pacific Branch of Russian Federal Institute of Fisheries and Oceanography (TINRO), Vladivostok, Primorskij kraj, Russia
Anna O. Zolotova*
Affiliation:
A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences (NSCMB FEB RAS), Vladivostok, Primorskij kraj, Russia
*
Corresponding author: Anna O. Zolotova; Email: anna.o.zolotova@gmail.com

Abstract

Squids of the family Gonatidae are key components in oceanic communities. However, issues related to correct species identification, number of species, and their genetic relatedness remain. To address these issues, sequences from three mitochondrial (cytochrome c oxidase subunit I [CO1], 16S rRNA, and 12S rRNA) and two nuclear (18S and 28S) genes were analysed in the Gonatidae. Four of the five sequences (12S rRNA, 16S rRNA, 28S, and CO1) yielded rather similar patterns of genetic relationships among the species. Molecular evidence suggested intra-familial subdivision into two major groups of species having either five or seven longitudinal rows of teeth in the radula. The former group included all species of the genus Gonatus and two sister-species of Gonatopsis s. str. suggesting that all gonatid species with five rows of radular teeth represent a single taxonomic unit of a genus or subfamily level. Species with seven rows of radular teeth formed several ‘species’ clusters. Sequence analysis also addressed species identification issues in the Gonatidae. Two genetically divergent groups were found among squid which conformed to the description of Gonatus berryi. Molecular evidence suggested sister-species relationships between ‘large’ and ‘small’ forms of Boreoteuthis borealis with size-at-maturity as the only reported difference between these two cohorts. Sequence variation was observed within Gonatus pyros. Inclusion of gonatid sequences from the GenBank into the analysis suggested probable species misidentification in several cases. Combined use of several mitochondrial and nuclear sequences served as a valuable tool for species identification and provided a solid background for unravelling molecular genetic and taxonomic relationships in the Gonatidae.

Type
Research Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afiati, N, Subagiyo, S, Handayani, CR, Hartati, R and Kholilah, N (2022) DNA barcoding on Indian Ocean squid, Uroteuthis duvaucelii (D'Orbigny, 1835) (Cephalopoda: Loliginidae) from the Java Sea, Indonesia. Jurnal Ilmiah Perikanan dan Kelautan 14, 231245.CrossRefGoogle Scholar
Aliabadian, M, Beentjes, KK, Roselaar, CS, van Brandwijk, H, Nijman, V and Vonk, R (2013) DNA barcoding of Dutch birds. ZooKeys 365, 2548.Google Scholar
Allcock, AL, Lindgren, AR and Strugnell, JM (2015) The contribution of molecular data to our understanding of cephalopod evolution and systematics: a review. Journal of Natural History 49, 13731421.CrossRefGoogle Scholar
Anderson, FE (2000) Phylogeny and historical biogeography of the loliginid squids (Mollusca: Cephalopoda) based on mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 15, 191214.CrossRefGoogle ScholarPubMed
Anderson, FE, Engelke, R, Jarrett, K, Valinassab, T, Mohamed, KS, Asokan, PK, Zacharia, PU, Nootmorn, P, Chotiyaputta, C and Dunning, M (2011) Phylogeny of the Sepia pharaonis species complex (Cephalopoda: Sepiida) based on analyses of mitochondrial and nuclear DNA sequence data. Journal of Molluscan Studies 77, 6575.CrossRefGoogle Scholar
Anderson, FE, Valinassab, T, Ho, CW, Mohamed, KS, Asokan, PK, Rao, GS, Nootmorn, P, Chotiyaputta, C, Dunning, M and Lu, CC (2007) Phylogeography of the pharaoh cuttle Sepia pharaonis based on partial mitochondrial 16S sequence data. Reviews in Fish Biology and Fisheries 17, 345352.CrossRefGoogle Scholar
Barr, NB, Cook, A, Elder, P, Molongoski, J, Prasher, D and Robinson, DG (2009) Application of a DNA barcode using the 16S rRNA gene to diagnose pest Arion species in the USA. Journal of Molluscan Studies 75, 187191.CrossRefGoogle Scholar
Berry, SS (1912) A review of the Cephalopods of Western North America. Bulletin of the Bureau of Fisheries 30, 267336.Google Scholar
Bolstad, KSR, Braid, HE, Strugnell, JM, Lindgren, AR, Lischka, A, Kubodera, T, Laptikhovsky, VL and Labiaga, AR (2018) A mitochondrial phylogeny of the family Onychoteuthidae Gray, 1847 (Cephalopoda: Oegopsida). Molecular Phylogenetics and Evolution 128, 8897.CrossRefGoogle Scholar
Bonnaud, L and Boucher-Rodoni, R (2002) Are 28S rDNA and 18S rDNA informative for cephalopod phylogeny? Bulletin of Marine Science 71, 197208.Google Scholar
Bonnaud, L, Boucher-Rodoni, R and Monnerot, M (1994) Phylogeny of decapod cephalopods based on partial 16S rDNA nucleotide sequences. Comptes Rendus de l Académie des Sciences – Series III – Sciences de la Vie 317, 581588.Google ScholarPubMed
Bonnaud, L, Lu, CC and Boucher-Rodoni, R (2006) Morphological character evolution and molecular trees in sepiids (Mollusca: Cephalopoda), is the cuttlebone a robust phylogenetic marker? Biological Journal of the Linnean Society 89, 139150.CrossRefGoogle Scholar
Bower, JR, Seki, K, Kubodera, T, Yamamoto, J and Nobetsu, T (2012) Brooding in a gonatid squid off Northern Japan. Biological Bulletin 223, 259262.CrossRefGoogle Scholar
Bublitz, C (1981) Systematics of the cephalopod family Gonatidae from the southeastern Bering Sea (PhD thesis). University of Alaska, Fairbanks, USA.Google Scholar
Canapa, A, Schiaparelli, S, Marota, I and Barucca, M (2003) Molecular data from the 16S rRNA gene for the phylogeny of Veneridae (Mollusca: Bivalvia). Marine Biology 142, 11251130.CrossRefGoogle Scholar
Carlini, DB (1998) The phylogeny of coleoid cephalopods inferred from molecular evolutionary analyses of the cytochrome c oxidase I, muscle actin, and cytoplasmic actin genes (PhD Dissertation). Virginia Institute of Marine Science, Gloucester Point, USA. doi: 10.25773/v5-3pyk-f023CrossRefGoogle Scholar
Carlini, DB and Graves, JE (1999) Phylogenetic analysis of cytochrome C oxidase I sequences to determine higher-level relationships within the coleoid cephalopods. Bulletin of Marine Science 64, 5776.Google Scholar
Chan, AHE, Saralamba, N, Saralamba, S, Ruangsittichai, J and Thaenkham, U (2022) The potential use of mitochondrial ribosomal genes (12S and 16S) in DNA barcoding and phylogenetic analysis of trematodes. BMC Genomics 23, 113. doi: 10.1186/s12864-022-08302-4CrossRefGoogle ScholarPubMed
Chen, J, Li, Q, Kong, LF and Yu, H (2011) How DNA barcodes complement taxonomy and explore species diversity: the case study of a poorly understood marine fauna. PLoS ONE 6, 19.CrossRefGoogle ScholarPubMed
Clarke, MR (1996) The role of cephalopods in the world's oceans: general conclusions and the future. Philosophical Transactions of the Royal Society B: Biological Sciences 351, 11051112.Google Scholar
Dai, L, Zheng, X, Kong, L and Li, Q (2012) DNA barcoding analysis of Coleoidea (Mollusca: Cephalopoda) from Chinese waters. Molecular Ecology Resources 12, 437447.CrossRefGoogle ScholarPubMed
Ekimova, IA, Antokhina, TI and Schepetov, DM (2020) Molecular data and updated morphological description of Flabellina rubrolineata (Nudibranchia: Flabellinidae) from the Red and Arabian seas. Ruthenica 30, 183194.CrossRefGoogle Scholar
Fahey, SJ (2003) Phylogeny of Halgerda (Mollusca: Gastropoda) based on combined analysis of mitochondrial CO1 and morphology. Invertebrate Systematics 17, 617624.CrossRefGoogle Scholar
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.CrossRefGoogle ScholarPubMed
Fernández-Álvarez, , Taite, M, Vecchione, M, Villanueva, R and Allcock, AL (2021) A phylogenomic look into the systematics of oceanic squids (order Oegopsida). Zoological Journal of the Linnean Society 20, 124.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Ghanimi, H, Goddard, JHR, Chichvarkhin, A, Gosliner, TM, Jung, DW and Valdés, A (2020) An integrative approach to the systematics of the Berthella californica species complex (Heterobranchia: Pleurobranchidae). Journal of Molluscan Studies 86, 186200.CrossRefGoogle Scholar
Giribet, G, Okusu, A, Lindgren, AR, Huff, SW, Schrödl, M and Nishiguchi, MK (2006) Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. PNAS 103, 77237728.CrossRefGoogle ScholarPubMed
Hall, TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hebert, P, Cywinska, A, Ball, S and de Waard, J (2003) Biological identifications through DNA barcodes. Proceedings. Biological Sciences 270, 313321.CrossRefGoogle ScholarPubMed
Hickerson, MJ, Meyer, CP and Moritz, C (2006) DNA barcoding will often fail to discover new animal species over broad parameter space. Systematic Biology 55, 729739.CrossRefGoogle ScholarPubMed
Hoving, HJT, Perez, JA, Bolstad, KS, Braid, HE, Evans, AB, Fuchs, D, Judkins, H, Kelly, JT, Marian, JE, Nakajima, R, Piatkowski, U, Reid, A, Vecchione, M and Xavier, JM (2014) The study of deep-sea cephalopods. Advances in Marine Biology 67, 235359.CrossRefGoogle Scholar
Jefferts, K (1983) Zoogeography and systematics of Cephalopods of the northeastern Pacific Ocean (PhD thesis). Oregon State University, Corvallis, USA.Google Scholar
Katugin, ON (2004) Squids of the family Gonatidae from the North Pacific Ocean and their genetic differentiation: controversial issues in the systematics and phylogeny. Ruthenica 14, 7387.Google Scholar
Katugin, ON, Chichvarkhina, OV, Zolotova, AO and Chichvarkhin, AY (2017) DNA barcoding for squids of the family Gonatidae (Cephalopoda: Teuthida) from the boreal North Pacific. Mitochondrial DNA Part A: DNA Mapping, Sequencing, and Analysis 28, 4149.CrossRefGoogle ScholarPubMed
Kizirian, D and Donnelly, MA (2004) The criterion of reciprocal monophyly and classification of nested diversity at the species level. Molecular Phylogenetics and Evolution 32, 10721076.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Lindgren, AR (2010) Molecular inference of phylogenetic relationships among Decapodiformes (Mollusca: Cephalopoda) with special focus on the squid order Oegopsida. Molecular Phylogenetics and Evolution 56, 7790.CrossRefGoogle ScholarPubMed
Lindgren, AR, Giribet, G and Nishiguchi, M (2004) A combined approach to the phylogeny of Cephalopoda (Mollusca). Cladistics 20, 454486.CrossRefGoogle Scholar
Lindgren, AR, Katugin, ON, Amezquita, E and Nishiguchi, M (2005) Evolutionary relationships among squids of the family Gonatidae (Mollusca: Cephalopoda) inferred from three mitochondrial loci. Molecular Phylogenetics and Evolution 36, 101111.CrossRefGoogle ScholarPubMed
Liu, J, Jiang, J, Song, S, Tornabene, L, Chabarria, R, Naylor, GJP and Li, C (2017) Multilocus DNA barcoding – species identification with multilocus data. Scientific Reports 7, 112. doi: 10.1038/s41598-017-16920-2Google ScholarPubMed
Lv, J, Wu, S, Zhang, Y, Chen, Y, Feng, C, Yuan, X, Jia, G, Deng, J, Wang, C, Wang, Q, Mei, L and Lin, X (2014) Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida). Parasites & Vectors 7, 111. doi: 10.1186/1756-3305-7-93CrossRefGoogle ScholarPubMed
Mabragaña, E, de Astarloa JM, D, Hanner, R, Zhang, J and González Castro, M (2011) DNA barcoding identifies argentine fishes from marine and brackish waters. PLoS ONE 6, 111. doi: 10.1371/journal.pone.0028655CrossRefGoogle ScholarPubMed
Machida, RJ and Knowlton, N (2015) Correction: PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PLoS ONE 10, e0134314.CrossRefGoogle ScholarPubMed
Maggioni, D, Tatulli, G, Montalbetti, E, Tommasi, N, Galli, P, Labra, M, Pompa, PP and Galimberti, A (2020) From DNA barcoding to nanoparticle-based colorimetric testing: a new frontier in cephalopod authentication. Applied Nanoscience 10, 10531060.CrossRefGoogle Scholar
Meyer, A, Todt, C, Mikkelsen, NT and Lieb, B (2010) Fast evolving 18S rRNA sequences from Solenogastres (Mollusca) resist standard PCR amplification and give new insights into mollusk substitution rate heterogeneity. BMC Evolutionary Biology 10, 112. doi: http://www.biomedcentral.com/1471-2148/10/70CrossRefGoogle ScholarPubMed
Naef, A (1923) Die Cephalopoden. In Naef, A (ed.), Fauna und Flora des Golfes von Neapel und der Angrenzenden Meeres-Abschnitte. Berlin: R. Friedländer & Sohn, pp. 149863.Google Scholar
Neigel, J, Domingo, A and Stake, J (2007) DNA barcoding as a tool for coral reef conservation. Coral Reefs 26, 487499.CrossRefGoogle Scholar
Nesis, KN (1973) Taxonomy, phylogeny and evolution of squids of the family Gonatidae. Zhoologicheskij Zhurnal 52, 16261639 (in Russian, with English summary).Google Scholar
Nesis, KN (1987) Cephalopods of the World: Squids, Cuttlefishes, Octopuses, and Allies. Neptune City: TFH Publications.Google Scholar
Nesis, KN (1989) Teuthofauna of the Okhotsk Sea. Biology of squids Berryteuthis magister and Gonatopsis borealis (Gonatidae). Zoology Journal 68, 4556 (in Russian, with English summary).Google Scholar
Nesis, KN (1997) Gonatid squids in the subarctic north pacific ecology, biogeography, niche diversity and role in the ecosystem. Advances in Marine Biology 32, 243324.CrossRefGoogle Scholar
Nesis, KN and Nezlin, NP (1993) Intraspecific groupings of gonatid squids. Russian Journal of Ecology 2, 91102.Google Scholar
Okutani, T (1968) Review of Gonatidae (Cephalopoda) from the North Pacific. Venus 27, 3134 (in Japanese).Google Scholar
Okutani, T and Clarke, MR (1992) Family Gonatidae, Hoyle 1886. In Sweeney, MJ, Roper, CFE, Mangold, KM, Clarke, MR and Boletzky, SV (eds), ‘Larval’ and Juvenile Cephalopods: A Manual for their Identification. Washington, DC: Smithsonian Institution Press, pp. 139156.Google Scholar
Okutani, T, Kubodera, T and Jefferts, K (1988) Diversity, distribution and ecology of gonatid squids in the Subarctic Pacific. A review. Bulletin of the Ocean Research Institute 26, 159192.Google Scholar
Palumbi, SR, Martin, AP, Romano, SL, McMillan, WO, Stice, L and Grabowski, G (1991) The Simple Fool's Guide to PCR, 2nd edn. Honolulu City: University of Hawaii.Google Scholar
Pearcy, WG and Voss, GL (1963) A new species of gonatid squid from the northeastern Pacific. Proceedings of the Biological Society of Washington 76, 105112.Google Scholar
Plazzi, F and Passamonti, M (2010) Towards a molecular phylogeny of mollusks: bivalves’ early evolution as revealed by mitochondrial genes. Molecular Phylogenetics and Evolution 57, 641657.CrossRefGoogle ScholarPubMed
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.CrossRefGoogle ScholarPubMed
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 18641877.CrossRefGoogle ScholarPubMed
Puslednik, L and Serb, JM (2008) Molecular phylogenetics of the Pectinidae (Mollusca: Bivalvia) and effect of increased taxon sampling and outgroup selection on tree topology. Molecular Phylogenetics and Evolution 48, 11781188.CrossRefGoogle ScholarPubMed
Roldán, MI, Planella, L, Heras, S and Fernández, MV (2014) Genetic analyses of two spawning stocks of the short-finned squid (Illex argentinus) using nuclear and mitochondrial data. Comptes Rendus – Biologies 337, 503512.CrossRefGoogle ScholarPubMed
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 15721574.Google ScholarPubMed
Roper, CFE, Jorgensen, EM, Katugin, ON and Jereb, P (2010) Family Gonatidae Hoyle, 1886. In Jereb, P and Roper, CFE (eds), Cephalopods of the World: An Annotated and Illustrated Catalogue of Cephalopod SPECIES Known to Date, Vol. 2. Myopsid and Oegopsid Squids. Rome: FAO, pp. 200222 (FAO species catalogue for fisheries purposes, no. 4).Google Scholar
Sanchez, G, Setiamarga, DHE, Tuanapaya, S, Tongtherm, K, Winkelmann, IE, Schmidbaur, H, Umino, T, Albertin, C, Allcock, L, Perales-Raya, C, Gleadall, I, Strugnell, JM, Simakov, O and Nabhitabhata, J (2018) Genus-level phylogeny of cephalopods using molecular markers: current status and problematic areas. PeerJ 6, 119. doi: 10.7717/peerj.4331Google ScholarPubMed
Sanchez, G, Tomano, S, Umino, T, Wakabayashi, T and Sakai, M (2016) Evaluation of the 5′ end of the 16S rRNA gene as a DNA barcode marker for the Cephalopoda. Fisheries Science 82, 279288.CrossRefGoogle Scholar
Savinykh, VF (2005) Main results of pelagic fishes and squids studies in TINRO Center. Izvestia TINRO 141, 146172.Google Scholar
Schröder, HC, Efremova, SM, Itskovich, VB, Belikov, S, Masuda, Y, Krasko, A, Müller, M and Müller, WEG (2003) Molecular phylogeny of the freshwater sponges in Lake Baikal. Journal of Zoological Systematics and Evolutionary Research 41, 8086.CrossRefGoogle Scholar
Seibel, BA, Hochberg, FG and Carlini, DB (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea), deep-sea spawning and post-spawning egg care. Marine Biology 137, 519526.CrossRefGoogle Scholar
Shearer, TL, Van Oppen, MJH, Romano, SL and Wörheide, G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 24752487.CrossRefGoogle ScholarPubMed
Spasojevic, T, Kropf, C, Nentwig, W and Lasut, L (2016) Combining morphology, DNA sequences and morphometrics: revising closely related species in the ord-weaving spider genus Araniella (Araneae, Araneidae). Zootaxa 4111, 448470.CrossRefGoogle ScholarPubMed
Taite, M, Vecchione, M, Fennell, S and Allcock, AL (2020) Paralarval and juvenile cephalopods within warm-core eddies in the North Atlantic. Bulletin of Marine Science 96, 235261.CrossRefGoogle Scholar
Takumiya, M, Kobayashi, M, Tsuneki, K and Furuya, H (2005) Phylogenetic relationships among major species of Japanese coleoid cephalopods (Mollusca: Cephalopoda) using three mitochondrial DNA sequences. Zoological Science 22, 147155.CrossRefGoogle ScholarPubMed
Tan, K and Conaco, C (2021) Characterization of the hidden break in giant clam 28S ribosomal RNA. Journal of Molluscan Studies 87, eyab029.CrossRefGoogle Scholar
Tkach, VV, Curran, SS, Bell, JA and Overstreet, RM (2013) A new species of Crepidostomum (Digenea: Allocreadiidae) from Hiodon tergisus in Mississippi and molecular comparison with three congeners. Journal of Parasitology 99, 11141121.CrossRefGoogle ScholarPubMed
Vecchione, M, Young, RE and Piatkowski, U (2010) Cephalopods of the northern mid-Atlantic ridge. Marine Biology Research 6, 2552.CrossRefGoogle Scholar
Vences, M, Thomas, M, van der Meijden, A, Chiari, Y and Vieites, DR (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology 2, 112.CrossRefGoogle ScholarPubMed
Wen, J, Tinacci, L, Acutis, PL, Riina, MV, Xu, Y, Zeng, L, Ying, X, Chen, Z, Guardone, L, Chen, D, Sun, Y, Zhao, J, Guidi, A and Armani, A (2017) An insight into the Chinese traditional seafood market: species characterization of cephalopod products by DNA barcoding and phylogenetic analysis using COI and 16S rRNA genes. Food Control 84, 333342.CrossRefGoogle Scholar
Young, RE (1972) The Systematics and Areal Distribution of Pelagic Cephalopods from the Seas off Southern California. Washington, DC: Smithsonian Institution Press.CrossRefGoogle Scholar
Zubakov, D, Sherbakov, D and Sitnikova, T (1997) Phylogeny of the endemial Baicaliidae molluscs inferred from partial nucleotide sequences of the CO1 mitochondrial gene. Molecular Biology 31, 935939 (in Russian).Google Scholar
Zuev, MA, Katugin, ON, Shevtsov, GA and Dakus, AV (2007) Distribution and differentiation of the Boreo Pacific gonate squid Boreoteuthis borealis (Sasaki, 1923) (Cephalopoda: Gonatidae) in the Okhotsk Sea and North Western Pacific Ocean. Proceedings of VNIRO 147, 266283 (in Russian, with English summary).Google Scholar
Supplementary material: File

Katugin and Zolotova supplementary material

Katugin and Zolotova supplementary material

Download Katugin and Zolotova supplementary material(File)
File 78 KB