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Cryptic biodiversity in the commercial diamondback squid Thysanoteuthis rhombus Troschel 1857

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Abstract

Cephalopod fisheries are increasing, but little is known about the cryptic diversity of some key commercial species. Recent studies have shown that cryptic speciation is common in cephalopods, including several oceanic squids formerly considered ‘cosmopolitan species.’ Further efforts are needed to investigate the cryptic diversity of commercial species, to inform management and support sustainable fisheries practices. Thysanoteuthis rhombus is an oceanic squid, currently recognized as the single species of the family Thysanoteuthidae. Thysanoteuthis. rhombus has a global distribution in tropical and subtropical waters and is an economically important species, with the highest catches occurring off Okinawa in Japan and of potential fishery resource for other countries due to its high abundance and large size. Here, we used sequences from 12S rRNA, 16S rRNA, and cytochrome c oxidase I to characterize its cryptic diversity using samples collected throughout most of its known geographic range. We identified three different putative species whose distributions are concordant with main ocean basins: Thysanoteuthis major, the most abundant species, is widely distributed in the North Pacific Ocean, North Indian Ocean, and limits of the South Atlantic Ocean; Thysanoteuthis rhombus is distributed in the North and South Atlantic Ocean and Mediterranean Sea; and Thysanoteuthis cf. filiferum, likely the least sampled to date, is found in the southwestern Pacific Ocean. A sister relationship was observed between T. rhombus and T. major, and T. cf. filiferum was found to be the most divergent species. Based on our divergence estimation, we hypothesize that the closure of the Isthmus of Panama during the early Pliocene played a significant role in the split of T. rhombus and T. major, while the split of their ancestor from T. cf. filiferum coincided with an increase in the Pacific Walker Circulation and the longitudinal gradient of surface temperatures in the Pacific Ocean during the Late Oligocene and Early Miocene. Our work identifies three different putative species within Thysanoteuthis and has potential use for improving fishery management and conserving the diversity in these species.

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Data availability

Alignments and raw data generated can be found in FigShare (https://doi.org/10.6084/m9.figshare.22559374). All the new sequences generated here are in the National Center for Biotechnology Information (NCBI) database under the GenBank accession numbers OP970836-OP970872 (cytochrome oxidase c subunit I.), OP970877-OP970912 (16S ribosomal RNA), and OP971221-OP971257 (12S ribosomal RNA).

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Acknowledgements

We thank Professor Umino Tetsuya from Hiroshima University for his support during this project. We also want to thank to Atsushi Tsuyuki and Honoka Arita for their help with collection logistics. D.D. was supported by The Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT) fellowship. G.S. wants to thank the support of the 22K15085 Grant-in-Aid for Early-Career Scientists (KAKENHI). F.Á.F.-Á. was supported by a JdC-I Postdoctoral Fellowship Grant (ref. IJC2020-043170-I) awarded by MCIN/AEI https://doi.org/10.13039/501100011033, by a Beatriu de Pinós fellowship from Secretaria d'Universitats i Recerca del Departament de Recerca i Universitats of the Generalitat de Catalunya (Ref. BP 2021 00035), the project ECOPHYN (Ref. PID2021-126824NB-C32, Ministerio de Ciencia e Innovación, Gobierno de España) and the European Union and the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S). A.E was supported by a Margarita Salas Postdoctoral Fellowship Grant awarded by Ministry of Universities of Spanish government and is thankful to the support of project DEEPCOM (Ref. CTM2017-88686-P, Ministerio de Ciencia e Innovación, Gobierno de España). We are thankful to the Director of ICAR-CMFRI, Kochi, India for facilities and support. CH. S. is thankful to the support of the JSPS KAKENHI Grant-in-Aid for Early-Career Scientists, Grant Number 19K15901. Thanks to the New Zealand Scientific Observer Programme, which is funded by the New Zealand Ministry for Primary Industries, for specimen collection.

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DD generated and analysed the data and wrote the manuscript under the supervision of GS. SM and KK executed the experiments and generated data. AE, AM, FL, HB, JGM, KKS, KSohamed, KM, ChS, FÁFÁ, and GS provided samples and edited the manuscript. GS and FÁFÁ supervised the study, designed the research, and provided funding. All the authors reviewed and approved the final manuscript.

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Correspondence to Fernando Á. Fernández-Álvarez or Gustavo Sanchez.

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Deville, D., Mori, S., Kawai, K. et al. Cryptic biodiversity in the commercial diamondback squid Thysanoteuthis rhombus Troschel 1857. Rev Fish Biol Fisheries 34, 293–313 (2024). https://doi.org/10.1007/s11160-023-09813-3

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