Abstract
The population structure and demographic history of a pelagic lumpsucker, Aptocyclus ventricosus, were investigated on the basis of sequence variation in the mitochondrial cytochrome b gene (1038 bp). The haplotype network clearly recovered two haplotype groups, consisting of western and eastern North Pacific individuals, except for some specimens collected from offshore of Tohoku, northern Japan. The geographic distribution of haplotypes suggests that the ocean currents in the North Pacific have shaped the population structure of the species after historical vicariant events between the Kuril Islands and Kamchatka Peninsula. In addition, the demographic histories of the two haplotype groups were quite different, suggesting that the western North Pacific group experienced a population expansion starting around 10,000 years ago, while the population size of the eastern North Pacific group has remained more stable.
References
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comp Biol 10:e1003537
Canino MF, Spies IB, Cunningham KM, Hauser L, Grant WS (2010) Multiple ice-age refugia in Pacific cod, Gadus macrocephalus. Mol Ecol 19:4339–4351
Davenport J (1985) Synopsis of biological data on the lumpsucker Cyclopterus lumpus (Linnaeus, 1758). FAO Fish Synop 147:1–31
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Fujita J, Drumm DT, Iguchi A, Ueda Y, Yamashita Y, Ito M, Tominaga O, Kai Y, Yamashita Y (2017) Deep-sea phylogeographic structure shaped by paleoenvironmental changes and ongoing ocean currents around the sea of Japan in a crangonid shrimp, Argis lar. Zool Sci 34:406–414
Garcia-Mayoral E, Olsen M, Hedeholm R, Post S, Nielsen EE, Bekkevold D (2016) Genetic structure of West Greenland populations of lumpfish Cyclopterus lumpus. J Fish Biol 89:2625–2642
Grant WAS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biol 66:591–600
Hedeholm R, Blicher ME, Grønkjær P (2014) First estimates of age and production of lumpsucker (Cyclopterus lumpus) in Greenland. Fisher Res 149:1–4
Kai Y, Orr JW, Sakai K, Nakabo T (2011) Genetic and morphological evidence for cryptic diversity in the Careproctus rastrinus species complex (Liparidae) of the North Pacific. Ichthyol Res 58:143–154
Kai Y, Stevenson DE, Ueda Y, Hamatsu T, Nakabo T (2015) Molecular insights into geographic and morphological variation within the Eumicrotremus asperrimus species complex (Cottoidei: Cyclopteridae). Ichthyol Res 62:396–408
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kyûshin K (1975) The embryonic and larval development, growth, survival and changes in body form, and the effect of temperature on these characteristics of the smooth lumpsucker, Aptocyclus ventricosus (Pallas). Bull Fac Fish Hokkaido Univ 26:49–72
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116
Mecklenburg CW, Sheiko BA (2003) Family Cyclopteridae Bonaparte 1831-lumpsuckers. Calif Acad Sci, Ann Checklists Fish 6:1–17
Mecklenburg CW, Mecklenburg TA, Thorsteinson LK (2002) Fishes of Alaska. American Fisher Society, Bethesda, Maryland
Nakabo T, Kai Y (2013) Cyclopteridae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, 3rd ed. Tokai Univ Press, Hadano, pp 1202–1204, 2071–2072
Nishimura S (1983) Okhotsk Sea, Japan Sea, East China Sea. In: Ketchum BH (ed) Ecosystems of the world, vol 26, estuarine and enclosed seas. Elsevier, Amsterdam, pp 375–401
Okazaki Y, Takahashi K, Katsuki K, Ono A, Hori J, Sakamoto T, Uchida M, Shibata Y, Ikehara M, Aoki K (2005) Late Quaternary paleoceanographic changes in the southwestern Okhotsk Sea: evidence from geochemical, radiolarian, and diatom records. Deep Sea Res II: Topical Stud Oceanog 52:2332–2350
Okiyama M (2004) Deepest demersal fish community in the sea of Japan: a review. Contrib from Biol Lab Kyoto Univ 29:409–429
Oku K, Imamura H, Yabe M (2017) Phylogenetic relationships and a new classification of the family Cyclopteridae (Perciformes: Cottoidei). Zootaxa 4222:1–59
Pampoulie C, Skirnisdottir S, Olafsdottir G, Helyar SJ, Thorsteinsson V, Jónsson SÞ, Fréchet A, Durif CMF, Sherman S, Lampart-Kałużniacka M, Hedeholm R, Ólafsson H, Daníelsdóttir AK, Kasper JM (2014) Genetic structure of the lumpfish Cyclopterus lumpus across the North Atlantic. ICES J Mar Sci 71:2390–2397
Qiu B (2010) Kuroshio and Oyashio currents. In: Steele JH, Thorpe SA, Turekian KK (eds) Ocean currents: a derivative of the encyclopedia of ocean sciences, 2nd edn. Academic Press, Cambridge, pp 61–72
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Sakuma K, Ueda Y, Hamatsu T, Kojima S (2014) Contrasting population histories of the deep-sea demersal fish, Lycodes matsubarai, in the sea of Japan and the Sea of Okhotsk. Zool Sci 31:375–382
Shirai SM, Kuranaga R, Sugiyama H, Higuchi M (2006) Population structure of the sailfin sandfish, Arctoscopus japonicus (Trichodontidae), in the sea of Japan. Ichthyol Res 53:357–368
Smith WL, Busby MS (2014) Phylogeny and taxonomy of sculpins, sandfishes, and snailfishes (Perciformes: Cottoidei) with comments on the phylogenetic significance of their early-life-history specializations. Mol Phylogenet Evol 79:332–352
Solomatov SF, Orlov AM (2018) Smooth lumpsucker Aptocyclus ventricosus in the northwestern sea of Japan: distribution and some life history traits. Archi Polish Fisher 26:5–20
Stevenson DE, Mecklenburg CW, Kai Y (2017) Taxonomic clarification of the Eumicrotremus asperrimus species complex (Teleostei: Cyclopteridae) in the eastern North Pacific. Zootaxa 4294:419–435
Tabata R, Kakioka R, Tominaga K, Komiya T, Watanabe K (2016) Phylogeny and historical demography of endemic fishes in Lake Biwa: the ancient lake as a promoter of evolution and diversification of freshwater fishes in western Japan. Ecol Evol 6:2601–2623
Tada R (1994) Paleoceanographic evolution of the Japan Sea. Palaeogeog Palaeoclimatol, Palaeoecol 108:487–508
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tokairin A, Kai Y, Ueda Y, Hamatsu T, Ito M, Nakabo T (2016) Genetic population structure of Crystallichthys matsushimae (Cottoidei: Liparidae) with comments on color variation. Ichthyol Res 63:370–381
Tyler PA (2002) Deep-sea eukaryote ecology of the semi-isolated basins off Japan. J Oceanog 58:333–341
Whittaker BA, Consuegra S, de Leaniz CG (2018) Genetic and phenotypic differentiation of lumpfish (Cyclopterus lumpus) across the North Atlantic: implications for conservation and aquaculture. PeerJ 6:e5974
Yoshida H (2003) Aptocyclus ventricosus. In: Ueda Y, Maeda K, Shimada H, Takami T (eds) Fisheries and aquatic life in Hokkaido. The Hokkaido Shinbun Press, Sapporo, pp 45–48
Yoshida H, Yamaguchi H (1985) Distribution and feeding habits of the pelagic smooth lumpsucker, Aptocyclus ventricosus (Pallas), in the Aleutian Basin. Bull Fac Fisher Hokkaido Univ 36:200–209
Acknowledgements
We sincerely thank K. Fujiwara (Japan Sea National Fisheries Research Institute), the crews of T/V Tanshu-maru (Kasumi High School) and R/V Kaiyo-maru No. 5, O. Tsuruoka (Akkeshi Shoyo High School), and the Groundfish Assessment Program at the Alaska Fisheries Science Center for their help in the collection of specimens. We also greatly appreciate the curatorial assistance of F. Tashiro, R. Misawa (formerly FAKU) and K.P. Maslenikov (UW). This study was supported in part by JSPS KAKENHI (Grant Number: 19 K06808) and the Fisheries Agency of Japan under the projects of “Assessment of Fisheries Stocks in the Waters around Japan.”
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Okazaki, T., Stevenson, D.E., Kai, Y. et al. Genetic population structure and demographic history of a pelagic lumpsucker, Aptocyclus ventricosus. Environ Biol Fish 103, 283–289 (2020). https://doi.org/10.1007/s10641-020-00955-y
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DOI: https://doi.org/10.1007/s10641-020-00955-y