Phylogeography of the North Pacific Lightfish Maurolicus Japonicus
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Plankton Benthos Res 13(4): 180–184, 2018 Plankton & Benthos Research © The Plankton Society of Japan Note Phylogeography of the North Pacific lightfish Maurolicus japonicus 1,2,† 2,†† 3 4 1,2, RYUSUKE TERADA , TSUYOSHI TAKANO , KAY SAKUMA , YOJI NARIMATSU & SHIGEAKI KOJIMA * 1 Graduate School of Frontier Sciences, the University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8563, Japan 2 Atmosphere and Ocean Research Institute, the University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8564, Japan 3 Japan Sea National Fisheries Research Institute, Fisheries Research and Education Agency, Japan, 1–5939–22 Suido-cho, Niigata 951–8121, Japan 4 Tohoku National Fisheries Institute, Fisheries Research and Education Agency, Japan, 3–27–5 Shinhama-cho, Shiogama, Miyagi 985–0001, Japan † Present address: IDEA Consultant Inc., 3–15–1 Komazawa, Tokyo 154–8585, Japan †† Present address: Meguro Parasitological Museum, 4–1–1 Shimomeguro, Meguro, Tokyo 153–0064, Japan Received 13 November 2017; Accepted 26 February 2018 Responsible Editor: Ryuji Machida doi: 10.3800/pbr.13.180 Abstract: A total of 113 and 73 individuals of the North Pacific lightfish Maurolicus japonicus were collected from the Japan Sea and the Pacific Ocean off the Japanese Islands, respectively. Based on nucleotide sequences of mitochondrial genes for cytochrome oxidase c subunit I (COI) and 16S ribosomal RNA, they were classified into the ‘Southern’ clade by Rees et al. (2017). Taken together, the previous results and our present findings suggest that the individuals examined should be treated as a single species, Maurolicus australis, and that this species exhibits the highest genetic diversity in the North Western Pacific Ocean. The Japanese population con- sisted of three genetically distinct groups. Individuals of one group are also distributed in the South Eastern Atlantic and the Southern Pacific Oceans, and individuals of another group are also distributed in the North Eastern Pacific Ocean. The remaining group has not yet been reported from other sea areas and might be endemic to the North Western Pacific. Although no significant genetic structure was detected around the Japanese Islands, the frequencies of these three groups seemed to show a latitudinal trend. Key words: Japan Sea, Maurolicus australis, Maurolicus japonicus, North Pacific lightfish, Pacific Ocean, phylogeography The Japan Sea is one of the marginal seas of the Asian demersal fishes (Lycodes japonicus Matsubara & Iwai, 1951; Continent (Fig. 1) and is connected to neighboring seas Careproctus notosaikaiensis Kai, Ikeguchi & Nakabo, 2011) through narrow, shallow straits. The deep-sea fauna of this and snails (Buccinum striatissimum Sowerby, 1899; Buccinum region is known to have been affected by environmental tsubai Kuroda & Kikuchi, 1933) are known to be endemic changes during the glacial periods. During the last glacial to the Japan Sea (Amano 2004, Iguchi et al. 2007, Kai et maximum (LGM), most deep-sea animals went extinct due al. 2011b, Sakuma et al. 2015), no endemic mesopelagic fish to anoxidation affecting most of the sea (Itaki et al. 2004). have been reported. The North Pacific lightfish Maurolicus However, some species without ontogenetic vertical migra- japonicus Ishikawa, 1915 is the sole mesopelagic fish that tion̶such as the Japan Sea eelpout Bothrocara hollandi reproduces in the Japan Sea (Okiyama 1971). Besides the Ja- (Jordan & Hubbs, 1925) and snailfishes of the genus Care- pan Sea, M. japonicus also inhabits the East China Sea and proctus̶survived the LGM in the Japan Sea (Kodama et al. the North Pacific Ocean around the Japanese and Hawaiian 2008, Kai et al. 2011a, Kojima et al. 2011). After the LGM, Islands (Aizawa & Doiuchi 2013). Aizawa & Doiuchi (2013) the deep-sea animal colonization via these straits provided suggested the possibility that Maurolicus fish inhabiting wa- the fauna in this sea area some unique characteristics such ters near the Hawaiian Islands are not M. japonicus based on as low endemism, low species diversity, wider habitat depth their geographical remoteness. ranges of species than the neighboring areas, and an almost Taxonomy of the genus Maurolicus has been muddled for complete lack of typical deep-sea groups, e.g., lantern fishes a long time, as Maurolicus fishes show almost no interspe- and rattails (Nishimura 1983, Okiyama 2004). While a few cific difference in the number and arrangement of the lumi- nous organs, which are used as taxonomic characters for other * Corresponding author: Shigeaki Kojima; E-mail, [email protected] mesopelagic fishes. Therefore, these fish have been classified tokyo.ac.jp based on other morphological traits that sometimes exhibit Phylogeography of Maurolicus japonicus 181 high intraspecifc variation and a large overlap among species, (Folmer et al. 1994), and 16Sar (5′-CGC CTG TTT ATC AAA leading to much confusion. Grey (1964) unified all of the six AAC AT-3′) and 16Sbr (5′-CCG GTC TGA ACT CAG ATC described species into a single valid species Maurolicus muel- ACG T-3′) (Palumbi 1996), respectively. The steps used to leri (Gmelin, 1789). Parin & Kobyliansky (1993) revised this perform PCR were as follows: incubation at 94°C for 120 s, genus to recognize 15 valid species including M. japonicus. followed by 35 cycles at 94°C for 40 s, 54°C for 60 s, and 72°C Based on nucleotide sequences of mitochondrial genes for cy- for 90 s. To degrade the remaining primers and nucleotides, tochrome oxidase c subunit I (COI) and 16S ribosomal RNA 5 µL of the PCR products was mixed with 1 µL of ExoSAP-IT (16S) and nuclear internal transcribed spacer region 2 (ITS-2) (United States Biochemical, Cleveland, OH, USA) and incu- sequences, Rees et al. (2017) reported that five of the Mauro- bated at 37°C for 15 min and 80°C for 15 min. Each purified licus species can be classified into three genetically distinct PCR product was used in cycle sequence reactions with the clades: the ‘Southern,’ ‘Northern,’ and ‘Equatorial/Western same primers as for PCR, using a BigDye Terminator Cycle North Atlantic’ clades. Although M. japonicus was not includ- Sequencing Kit, version 3.0 (Applied Biosystems, Foster City, ed in their study, Rees et al. (2017) suspected that this species CA, USA). The nucleotide sequences were determined bi- belongs to the ‘Southern’ clade, which consists of Maurolicus directionally using an ABI 3130 automated DNA sequencer walvisensis Parin & Kobyliansky, 1993 from the South East- (Applied Biosystems). The nucleotide sequences determined ern Atlantic Ocean and Maurolicus australis Hector, 1875 in the current study were deposited in the DDBJ/EMBL/ from the Southern Pacific Ocean, as Kim et al. (2008) and GenBank databases under the accession numbers LC371262– Habib et al. (2012) suggested synonymy between M. japoni- 371273 (COI) and LC371274–371280 (16S). Additional se- cus and M. walvisensis based on 16S sequences and morphol- quence data of M. japonicus from the most southeastern part ogy. Rees et al. (2017) further suggested these three species of the Japan Sea, M. australis from the Eastern Indian Ocean should be treated as a single species M. australis. During the and the Western South Pacific Ocean, M. walvisensis from present study, Maurolicus breviculus Parin & Kobyliansky, the Eastern Atlantic Ocean were referred from Suneetha et 1993 from the North Eastern Pacific Ocean off Panama was al. (2000), Kim et al. (2008), and Rees et al. (2017), with the shown to belong to the ‘Southern’ clade. Maurolicus brevicu- lus may also be a junior synonym of M. australis. A total of 113 and 73 individuals of M. japonicus were collected using an otter trawl during cruises of the training vessel (T/V) Tanshu-Maru of the Hyogo Prefectural Kasumi High School in the Japan Sea and the research vessel (R/V) Wakataka-Maru of the Tohoku National Fisheries Institute, Fisheries Research and Education Agency, Japan in the Pa- cific Ocean off the northeastern coast of the Japanese main- land (Honshu Island), respectively (Fig. 1, Table 1). A small piece of muscle tissue taken from each individual was stored in a freezer (−30°C) until used for molecular analyses. The remaining part of each specimen was fixed in 10% seawater formalin. Total DNA was extracted from frozen tissue using a DNeasy Tissue Extraction Kit (Qiagen, Valencia, CA) ac- cording to the manufacturer’s instructions. Mitochondrial DNA fragments including parts of COI and 16S genes were Fig. 1. Sampling sites of Maurolicus japonicus. Numbers of amplified through PCR using primer sets LCO1490 (5′- sampling sites are the same as those in Table 1. White, gray, and GGT CAA CAA ATC ATA AAG ATA TTG G-3′) and HCO black sectors in pie graphs indicate relative frequencies of indi- 2198 (5′-TAA ACT TCA GGG TGA CCA AAA AAT CA-3′) viduals belonging to groups C1, C2, and C3 in Fig. 2a, respectively. Table 1. List of sampling sites in the present study. No. Sea area Position Depth (m) N J1 off Shikotan Peninsula, the Japan Sea 43°10.17′N, 140°15.05′E 145 30 J2 off Noto Penunsula, the Japan Sea 37°41.93′N, 136°18.45′E 262 30 J3 Wakasa Bay, the Japan Sea 36°24.02′N, 135°46.18′E 383 23 J4 off Iki Islands, the Japan Sea 36°13.55′N, 133°44.58′E 247 30 P1 off Miyako, the Pacific Ocean 39°40.42′N, 142°12.48′E 213 13 P2 off Iwaki, the Pacific Ocean 37°22.41′N, 141°37.51′E 251 30 P3 off Joban, the Pacific Ocean 36°29.07′N, 140°15.05′E 246 30 182 R.TERADA et al. exception of a single 16S sequence of M. australis, which was harvested from GenBank (accession number: GQ860361). A COI sequence of Maurolicus breviculus Parin & Kobylian- sky, 1993 from the North Eastern Pacific Ocean off Panama (Sequence ID: LIDMA1145-12.COI-5P) was harvested from the Barcode of Life Data System (Ratnasingham & Hebert 2007).