Front. Mar. Sci. Frontiers in Marine Science Front. Mar. Sci. 2296-7745 Frontiers Media S.A. 10.3389/fmars.2022.1090034 Marine Science Perspective The geographic problem in cephalopod genomics Vecchione Michael 1 * Sweeney Michael J. 2 Rothman Paula L. 3 1 National Oceanic and Atmospheric Administration, National Marine Fisheries Service (NOAA/NMFS) National Systematics Lab., National Museum of Natural History, Washington, DC, United States 2 Retired, Durham, NC, United States 3 Department of Invertebrate Zoology, Smithsonian Museum of Natural History, Washington, DC, United States

Edited by: Michael J. Kuba, Okinawa International University, Japan

Reviewed by: Gianluca Polese, University of Naples Federico II, Italy; Anna Di Cosmo, University of Naples Federico II, Italy; Ryuta Nakajima, University of Minnesota Duluth, United States

*Correspondence: Michael Vecchione, vecchiom@si.edu

This article was submitted to Marine Evolutionary Biology, Biogeography and Species Diversity, a section of the journal Frontiers in Marine Science

 08 12 2022 2022 9 1090034 04 11 2022 21 11 2022 Copyright © 2022 Vecchione, Sweeney and Rothman 2022 Vecchione, Sweeney and Rothman

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Publications describing genomes of various cephalopod species have recently proliferated. Some papers have involved large geographic distances between the collection locality of sequenced specimens and the type locality of the presumed species. However, cryptic species have been demonstrated in many cephalopods. Therefore, even if the sequenced specimen is very similar morphologically to the species in question, the likelihood that it is a member of the species in question decreases with increasing distance from the type locality. An associated problem is that many publications do not provide information adequate to determine the source locality for the genomic sequence. We reviewed a decade of literature on mitochondrial genomes of cephalopods and found a total of 43 publications containing 48 species within 23 genera. Of the 48 species, only 17 could be evaluated for our geographic question. Distances between sampling locality and type locality of the named species ranged from 0 nautical miles (sampled at type locality) to half-way around the world. Where data were present for distance calculation, the average for the 17 species was 3785 km (2044 nmi).

 biogeography genomics species complex type locality sampling Introduction

Determination of genetic sequences has revolutionized understanding of evolutionary relationships. Increasingly sophisticated methods have allowed this revolution to progress greatly throughout the last few decades to include inferences about entire genomes. Accordingly, the literature describing cephalopod genomes, especially those of the mitochondria, has increased greatly over the past 10 years (O'Brien, 2018). The primary goal of most of these publications has been to resolve phylogenetic relationships within extant Cephalopoda.

Another result of widespread use of genetic sequencing, including “barcodes” and other sequences shorter than entire genomes, has been an increasing recognition that species with distributions once considered to be very broad or even global were actually complexes of morphologically similar species with geographic ranges resembling a patchwork within the broad range of the species complex. Some examples include taxa within the families Sepiolidae (Fernandez-Alvarez et al., 2021), Loliginidae (Sales et al., 2017), Chtenopterygidae (Escanez et al. (2018), Ommastrephidae (Fernandez-Alvarez et al., 2020; Xu et al., 2020a), Spirulidae (Hoffmann et al., 2021), and Octopodidae (Avendano et al., 2020; Amor and Hart, 2021). Because of these species complexes, both currently recognized and possibly to be discovered in the future, a substantial potential exists for misidentification of specimens collected for genomic sequencing (e.g., Lima et al., 2017; Salvi et al., 2021). This misidentification potential is especially true if the genomic specimen is not collected within the normal range of nominal sequenced species (i.e., named based on morphological identification). We are concerned that authors, using specimens from the nearest convenient area to sample a presumed species or from sources where the actual collection locality cannot be verified (e.g., fish markets, aquarium dealers), could be using a different species than what they report and, as a result, sequences in genomic databases may be misidentified.

 Materials and methods

We surveyed the past decade of genomic literature on Cephalopoda for comparison of collection locality with designated type localities of the nominal species to determine the extent of this potential problem. Only publications describing complete mitochondrial genomes were analyzed. Each publication was examined to determine the collection locality of the specimen used for genomic analysis. Type localities for the nominal species are available online. We converted both sample locality and type locality to latitude/longitude and then calculated distance between them using NOAA Latitude/Longitude Distance Calculator (https://www.nhc.noaa.gov/gccalc.shtml). The repository and accession numbers for published genome sequences were also recorded ( Table 1 ).

Mitochondrial genome sequences for cephalopods in recent literature.

Species Reference Genome repository Locality of specimen Type locality of species Separation*
Nautilus pompilius Wang et al., 2018 GenBank KY794928 Not given Ambon Island, Indonesia n/a
Sepia officinalis Akasaki et al., 2006 GenBank AB240155 Tsukiji Fishery Market, Japan "Oceano" [NE Atl. O.] n/a
Sepia aculeata Guo et al., 2016 GenBank KF690633 Not given Java, Indonesia n/a
Sepia apama Kawashima et al., 2013 GenBank AP013073 Not given Port Adelaide, Australia n/a
Sepia esculenta Yokobori et al., 2007 DDBJ genbank AB266516 Tsukiji Fishery Market, Japan Yokohama Fishery Market, Japan n/a
Sepia latimanus Kawashima et al., 2013 GenBank AP013074 Not given Port Dorey, New Guinea n/a
Sepia latimanus Lu et al., 2019 GenBank MK347498 Naozhou, China Port Dorey, New Guinea 1890
Sepia lycidas Kawashima et al., 2013 GenBank AP013075 Not given Canton Fishery Market, China n/a
Sepia lycidas Guo et al., 2018 GenBank KJ162574 Zhanjiang fishing grounds, SE China Canton Fishery Market, China n/a
Sepia pharaonis Kawashima et al., 2013 GenBank AP013076 Not given Gulf of Suez, Red Sea n/a
Sepia pharaonis Song et al., 2021 ERZ1300763 Ningbo City fishfarm, China Gulf of Suez, Red Sea n/a
Sepia pharaonis Wang et al., 2014 GenBank KC632521 Not given Gulf of Suez, Red Sea n/a
Metasepia tullbergi Lee et al., 2021 GenBank MT974497 NE Taiwan Nagasaki, Japan 632
Sepiella inermis Wang et al., 2015 GenBank KF040369 Not given Bombay [Mumbai], India n/a
Sepiella maindroni Zheng et al., 2016 GenBank KR912215.1 Not given Pondichery, India n/a
Semirossia patagonica Kawashima et al., 2013 GenBank AP012226 Not given Portland Bay, Patagonia n/a
Spirula spirula Strugnell et al., 2017 GenBank KU893141 Queensland, Australia America n/a
Loligo beka Jiang et al., 2016e & 2018 GenBank KT254309 30.1◦N 122.4◦E, E. China Sea Kojima Bay, Japan 585
Loligo chinensis Jiang et al., 2017b & 2018 GenBank KT362380 30.1◦N 122.4◦E, E. China Sea Canton Fishery Market, China n/a
Loligo duvauceli Jiang et al., 2016a & 2018 GenBank KR051264 30.1◦N 122.4◦E, E. China Sea Syntypes India & Sumatra n/a
Loligo edulis f. budo Takemoto & Yamashita, 2012 GenBank AB675081 Multiple locations Multiple locations, Japan n/a
Loligo edulis f. kensaki Takemoto & Yamashita, 2012 GenBank AB675080 Multiple locations Multiple locations, Japan n/a
Loligo japonica Jiang et al., 2017b & 2018 GenBank KU568467 Hakodate, Japan Yokohama Fishery Market, Japan n/a
Loligo opalescens Jiang et al., 2016d & 2018 GenBank KP336703 30.1◦N 122.4◦E, E. China Sea Puget Sound, Washington, USA 4975
Uroteuthis chinensis Xu et al., 2020b GenBank MN687903 Minnan–Taiwan Bank Canton Fishery Market, China n/a
Loliolus (N.) uyii Jiang et al., 2016b & 2018 GenBank KP265013 30.1◦N 122.4◦E, E. China Sea Kagoshima Bay, Japan 432
Sepioteuthis lessoniana Akasaki et al., 2006 GenBank AB240154 Tsukiji Fishery Market, Japan Not designated n/a
Watasenia scintillans Akasaki et al., 2006 GenBank AB240152 Tsukiji Fishery Market, Japan Misaki[?], Japan n/a
Watasenia scintillans Hayashi et al., 2016 GenBank KJ845633 Toyama Bay, Japan Misaki[?], Japan n/a
Chiroteuthis picteti H. Kim et al., 2018 GenBank MG833837 east sea of Korea Ambon Island, Indonesia 2450
Bathyteuthis abyssicola Kawashima et al., 2013 GenBank AP012225 Not given 46◦16'S 48◦27'E, Southern Ocean n/a
Thysanoteuthis rhombus Tang et al., 2021 GenBank MT733875 South China Sea Strait of Messina, Sicily 5070
Illex argentinus Jiang et al., 2016c GenBank KP336702 Not given Patagonia, 39◦S 55◦W n/a
Todarodes pacificus Akasaki et al., 2006 GenBank AB240153 Tsukiji Fishery Market, Japan Hokodate, Japan n/a
Sthenoteuthis oualaniensis Xu et al., 2020c GenBank MT661575 17◦59'N 111◦59'E, China Sea Oualan Island, Caroline Islands 3080
Vampyroteuthis infernalis Yokobori et al., 2007 DDBJ genbank AB266515 Ogasawara Island Chain, Japan 1◦56.7'S 7◦40.6'E, Atlantic Ocean 7715
Amphioctopus aegina Zhang et al., 2017 GenBank KT428877 Haikou Fishery Market, China Not designated n/a
Amphioctopus fangsiao Lashari et al., 2020 GenBank MF029678-029691 9 separate localities in China Japan n/a
Amphioctopus marginatus Tang et al., 2018 GenBank KY646153 Haikou Fishery Market, China Kamae, Oita Prefecture, Japan n/a
Amphioctopus neglectus Tang et al., 2019 GenBank MF447873 Nanning Fishery Market, China Ko Phuket, Thailand n/a
Amphioctopus rex Tang et al., 2019 GenBank MF447874 Wenzhon Fishery Market, China Ko Food, Trat Province, Thailand n/a
Octopus bimaculatus Dominguez et al., 2016 GenBank KT581981 N. Gulf of California, Mexico Syntypes; 3 localities n/a
Octopus conispadiceus Ma et al., 2016 GenBank KJ789854 Haishenwai, Amur Bay, Russia Sapparo Fishery Market, Japan n/a
Octopus dollfusi Yan et al., 2018 GenBank KX108697 Zhanjiang, Guangdong, China "Indochina" n/a
Octopus fitchi Magallon-Gayon et al., 2020 GenBank MK450541 Bahia Magdalena, Mexico N. Gulf of California, Mexico 990
Octopus minor B. Kim et al., 2018 SRA database SRX3462978 Not given Suruga Bay, Japan n/a
Octopus minor Cheng et al., 2012 GenBank HQ638215 Weihai, Shandong Province, China Suruga Bay, Japan 785
Octopus mimus Magallon-Gayon et al., 2020 GenBank MN078094 Zihuatanejo, Guerrero, Mexico Iquique, Chile 2925
Octopus ocellatus Akasaki et al., 2006 GenBank AB240156 Tsukiji Fishery Market, Japan "China Sea" n/a
Octopus sinensis Li et al., 2021 GenBank MT712046 Zhoushan, China Oyano Island, Ariake Sea, Japan 446
Octopus vulgaris Zarrella et al., 2019 Not listed Bay of Naples, Italy "Mediterranean Sea" n/a
Cistopus chinensis Cheng et al., 2013 GenBank KF017606 coastal Xiamen, China Xiamen, China 0!!
Cistopus taiwanicus Cheng et al., 2013 GenBank KF017605 "coastal Taiwan" Miaoli, Taiwan close+/-
Hapalochlaena fasciata Kim et al., 2020 GenBank MT497543 Southern coastal Korea Port Jackson, Australia 1165
Hapalochlaena maculosa Morse et al., 2018 Not listed 8 South Australia localities "Australia" n/a
Argonauta argo Hirota et al., 2021 DDBJ genbank LC596061 Oki Island, Sea of Japan Syntypes; Red Sea + Mediterranean n/a
Argonauta hians Chiu et al., 2018a GenBank KY649285 Kenting, Taiwan Ambon Island, Indonesia 1600
Tremoctopus violaceus Chiu et a.l, 2018b GenBank KY649286 Taiwan Not designated n/a

Approx. distance between specimen location and type locality calculated using https://www.nhc.noaa.gov/gccalc.shtml Separation* is calculated as nmi. (1nmi = 1.852 km). Shaded boxes: data absent or too general to be analyzed.

Bold numbers in the last column highlight the publications for which included information was adequate for distance calculation.

 Results

An online search of the previous ten years of Cephalopoda genomic literature found a total of 58 genomic descriptions within 43 publications containing 48 different species in 23 genera ( Table 1 ). For many species sequenced (70%), either collection locality or type locality (from the original description) was missing or was too general (e.g., Australia). In addition, if either locality was indeterminate (e.g., Tsukiji fishery market); or there were multiple type localities (ex. syntypes); or the genome was derived from combined specimens from multiple localities, the sequence was not included in our distance analysis.

Of the 48 species sequenced, only 17 could be evaluated for our geographic question ( Table 1 ). Distances calculated ranged from 0 km (sampled at type locality) to half-way around the world in a different ocean basin. The average distance between sampling locality and type locality for the 17 species for which data were adequate for distance calculation, was 3785 km (2044 nm).

Incidentally, as we reviewed this literature for geographic information, we also noticed that very few of the publications included any indication that voucher specimens or unprocessed tissue were preserved in established archival collections for future research. For example, of the 17 species mentioned above, only 5 (29.4%) had vouchered specimens. Thus, 10.4% of species accounts included both adequate geographic information and archived specimens.

 Discussion

Our point here is not that any of these publications is wrong. Rather, we want to highlight the potential for taxonomic errors in publications where the sampling area is very distant from the species’ type locality. As pointed out by one of the reviewers, for coastal cephalopod species in complex habitats, such errors are possible even at very small distances. Any taxonomic error introduced by this geographic mismatch may be compounded when the sequence is archived in a genomic database and the database is used for other investigations.

We therefore recommend selection of specimens for genomic sequencing collected from as close to the type locality of the species as possible. Although we recognize that it may not always be possible to sample the type locality, we recommend that the genomic sample be from the same biogeographic province (e.g., GOODS, 2009 or subsequent modifications by various authors) or “Large Marine Ecosystem” (LME – Sherman and Duda, 2011) as the type locality. The collecting locality should always be included in any publication resulting from DNA sequencing. Furthermore, specimens should not be selected for sequencing from a source where the actual collecting locality cannot be determined confidently (e.g., not from fishery landings, etc.). Also, although our primary purpose here is to highlight the need for sequenced specimens to come from as close to the type locality as possible, we also recommend that specimens sequenced and any unprocessed tissue be vouchered in an established archival collection. Relevant information about archived material (e.g., museum catalogue number) should be included in resulting publications.

 Data availability statement

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

 Ethics statement

Ethical review and approval was not required for the animal study because this is a literature review. No animals (live or preserved) were used.

 Author contributions

MS conceived the idea. MV and MS analyzed the data. PR accumulated the references. MV wrote the first draft. All authors contributed to the final manuscript. All authors contributed to the article and approved the submitted version.

 Funding

NOAA, NMFS which employs MV. US Gov’t is committed to open-access publication.

 Acknowledgments

The manuscript was improved by the comments from three reviewers and the Associate Editor.

 Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

 Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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