Ichthyological Research

, Volume 62, Issue 4, pp 396–408 | Cite as

Molecular insights into geographic and morphological variation within the Eumicrotremus asperrimus species complex (Cottoidei: Cyclopteridae)

  • Yoshiaki Kai
  • Duane E. Stevenson
  • Yuji Ueda
  • Tomonori Hamatsu
  • Tetsuji Nakabo
Full Paper


A molecular phylogeny of lumpsukers, Eumicrotremus asperrimus and related species (family Cyclopteridae), is presented on the basis of sequence variations in the cytochrome b and cytochrome c oxidase subunit 1 genes (1,659 base pairs) of mitochondrial DNA using specimens collected from across the North Pacific, including the Sea of Japan, Sea of Okhotsk, Bering Sea, and Gulf of Alaska. Specimens identified as Eumicrotremus phrynoides, Cyclopteropsis bergi, Cyclopteropsis lindbergi, and Lethotremus muticus on the basis of the presence or absence of spiny tubercles and height of the first dorsal fin did not exhibit reciprocal monophyly, but were randomly clustered with E. asperrimus. This collection of forms is therefore referred to as the “E. asperrimus species complex.” DNA sequence data presented here divided the E. asperrimus species complex into two distinct clades, corresponding to the eastern North Pacific (the Bering Sea, Aleutian Islands, and Gulf of Alaska) and the western North Pacific (the Seas of Japan and Okhotsk) regions. Slight morphometric differences between eastern and western clades were also evident, indicating that they represent at least two different species. The genetic level of divergence between the two clades suggests that the speciation event occurred during the early Pleistocene to late Pliocene. Although the presence and morphology of tubercles have been used extensively for species discrimination in Cyclopteridae, our results suggest that this character complex is confounded by intraspecific variation. Examined samples showed some sexual dimorphism in the relative development of the tubercles, although the pattern was different between the eastern and western North Pacific clades. These results underscore the need for a thorough re-examination of the taxonomy of Pacific cyclopterids, using molecular data to supplement potentially misleading tubercle morphology.


Mitochondrial DNA Cyclopteropsis Lethotremus North Pacific Phylogeography Spiny tubercles 



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, A. Yamasaki, T. Miyajima, and the crews of the R/V Heian-maru (Kyoto Prefectural Agriculture, Forestry and Fisheries Technology Center, Japan). We greatly appreciate the loans of specimens and gifts of tissues provided by T.W. Pietsch and K.P. Maslenikov (UW), as well as helpful discussions about statistics with J.W. Orr (AFSC). We also thank T.W. Pietsch and J.W. Orr for critical reviews of the manuscript. This study was supported in part by the Fisheries Agency of Japan under the projects of “Assessment of Fisheries Stocks in the Waters around Japan.”

Supplementary material

10228_2014_453_MOESM1_ESM.csv (12 kb)
Supplementary material 1 (CSV 11 kb)


  1. Aoyama J, Watanabe S, Ishikawa S, Nishida M, Tsukamoto K (2000) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161Google Scholar
  2. Arita GS (1969) Sexual dimorphism in the cyclopterid fish Eumicrotremus orbis. J Fisher Board Canada 26:3262–3265Google Scholar
  3. Belousov A, Belousova M, Miller T (2009) Kurile Islands. In: Encyclopedia of Islands. Eds. R. Gillespie and D. Clague. University of California Press, Berkeley, Los Angeles, London: 520-524Google Scholar
  4. Bezverkhniy VL, Pletnev SP, Nabiullin AA (2002) Outline of the geological structure and development of the Kuril Island System and adjacent regions. In: Storozhenko SY, Bogatov VV, Lelej AS (eds) Flora and fauna of the Kuril Islands: materials of the International Kuril Island Project. Dalnauka, Vladivostok, pp 35–66Google Scholar
  5. Briggs JC (1974) Marine zoogeography. McGraw-Hill book company, New YorkGoogle Scholar
  6. Briggs JC, Bowen BW (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. J Biogeogr 39:12–30Google Scholar
  7. Byrkjedal I, Rees DJ, Willassen EW (2007) Lumping lumpsuckers: molecular and morphological insights into the taxonomic status of Eumicrotremus spinosus (Fabricius, 1776) and Eumicrotremus eggvinii Koefoed, 1956 (Teleostei: Cyclopteridae). J Fish Biol 71 (suppl A):111–131Google Scholar
  8. Canino MF, Spies IB, Cunningham KM, Hauser L, Grant WS (2010) Multiple ice-age refugia in Pacific cod, Gadus macrocephalus. Mol Ecol 19:4339–4351Google Scholar
  9. Cantatore P, Roberti M, Pesole G, Ludovico A, Milella F, Gadaleta MN, Saccone C (1994) Evolutionary analysis of cytochrome b sequences in some Perciformes: evidence for a slower rate of evolution than in mammals. J Mol Evol 39:589–597Google Scholar
  10. Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto G, Mahardika GN, Manjaji-Matsumoto BM, Juinio-Menez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol Article ID 396982:1–14Google Scholar
  11. Chernova NV, Stein DL, Andriashev AP (2004) Family Liparidae Scopoli 1777—Snailfishes. Calif Acad Sci Annotated Checklist Fishes 31:1–72Google Scholar
  12. Davenport J (1985) Synopsis of biological data on the lumpsucker: Cyclopterus lumpus (Linnaeus, 1758), No. 147. FAO, RomaGoogle Scholar
  13. Dodson JJ, Tremblay S, Colombani F, Carscadden JE, Lecomte F (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species, the capelin (Mallotus villosus). Mol Ecol 16:5030–5043Google Scholar
  14. 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 Res 10:564–567Google Scholar
  15. Felsenstein J (1981) Evolutionary trees from DNA sequencies – a maximum-likelihood approach. J Mol Evol 17:368–376Google Scholar
  16. Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648Google Scholar
  17. Grant WS, Liu M, Gao TX, Yanagimoto T (2012) Limits of Bayesian skyline plot analysis of mtDNA sequences to infer historical demographies in Pacific herring (and other species). Mol Phylogenet Evol 65:203–212Google Scholar
  18. Harpending, HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600 Google Scholar
  19. Harrison PJ, Boyda PW, Varela DE, Takeda S, Shiomoto A, Odate T (1999) Comparison of factors controlling phytoplankton productivity in the NE and NW subarctic Pacific gyres. Prog Oceanog 43:205–234Google Scholar
  20. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular phylogenetics. J Mol Evol 22:160–174Google Scholar
  21. Ishiwatari R, Houtatsu M, Okada H (2001) Alkenone-sea surface temperatures in the Japan Sea over the past 36 kyr: warm temperatures at the last glacial maximum. Org Geochem 32:57–67Google Scholar
  22. 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 58:143–154Google Scholar
  23. Kai Y, Ueda Y, Fujiwara K, Itoh M, Yamasaki A, Nakabo T (2014) Population structure and demographic history of Davidijordania poecilimon (Perciformes: Zoarcidae). Species Diversity 19: in pressGoogle Scholar
  24. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:116–120Google Scholar
  25. Kitagawa D, Imamura H, Goto T, Ishito Y, Fujiwara K, Ueda Y (2008) Field guide of the fishes from the Tohoku district, north-eastern waters of Japan. Tokai University Press, HadanoGoogle Scholar
  26. Kodama Y, Yanagimoto T, Shinohara G, Hayashi I, Kojima S (2008) Deviation age of a deep-sea demersal fish, Bothrocara hollandi, between the Japan Sea and the Okhotsk Sea. Mol Phylogenet Evol 49:682–687 Google Scholar
  27. Lindberg GU, Legeza MI (1955) A review of the genera and species of subfamily Cyclopterinae (Pisces). Bull Zool Inst Acad Sci USSR 18:389–458Google Scholar
  28. Liu M, Lin LS, Gao TX, Yanagimoto T, Sakurai Y, Grant WS (2012) What Maintains the Central North Pacific Genetic Discontinuity in Pacific Herring? PloS One 7:e50340Google Scholar
  29. Liu JX, Tatarenkov A, Beacham TD, Gorbachev V, Wildes S, Avise JC (2011). Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii). Mol Ecol 20:3879–3893Google Scholar
  30. Mecklenburg CW, Mecklenburg TA, Thorsteinson LK (2002) Fishes of Alaska. American Fisher Soc, Bethesda, MarylandGoogle Scholar
  31. Mecklenburg CW, Sheiko BA (2003) Family Cyclopteridae Bonaparte 1831. Annotated Checklists Fish, Calf Acad Sci (6):1–17Google Scholar
  32. Meyer A (1993) Evolution of mitochondrial DNA in fishes. In: Hochachka PW, Mommsen TP (eds) Biochemistry and Molecular Biology of Fishes, Vol. 2. Elsevier, Amsterdam, pp. 1–38Google Scholar
  33. Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 34:134–146Google Scholar
  34. Nakabo T, Kai Y (2013) Cyclopteridae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, third edn. Tokai University Press, Tokyo, pp 665–677, 1529–1530Google Scholar
  35. Nelson JS (2006) Fishes of the world, 4th ed. John Wiley and Sons, New YorkGoogle Scholar
  36. Ortí G, Bell MA, Reimchen TE, Meyer A (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent migrations. Evolution 48:608–622CrossRefGoogle Scholar
  37. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The Simple Fool’s Guide to PCR. University of Hawaii Press, Honolulu, HawaiiGoogle Scholar
  38. Payne MC, Brown CA, Reusser DA, Lee HII (2012) Ecoregional analysis of nearshore sea-surface temperature in the North Pacific. PLoS One 7:e30105Google Scholar
  39. Rambaut A, Drummond AJ (2009) Tracer v1.5. Accessed 21 May
  40. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100Google Scholar
  41. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225Google Scholar
  42. Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theoret Biol 142:485–501Google Scholar
  43. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  44. Ronquist F, Huelsenbeck (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574Google Scholar
  45. Sakuma K, Ueda U, 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 31:375–382Google Scholar
  46. Shinohara G, Narimatsu Y, Hattori T, Ito M, Takata Y, Matsuura K (2009) Annotated checklist of deep-sea fishes from the Pacific coast off Tohoku District, Japan. In: Fujita T (ed) Deep-sea fauna and pollutants off Pacific coast of northern Japan. Natl Mus Nat Sci Monograph 39:683–735Google Scholar
  47. Shinohara G, Shirai SM, Nazarkin MV, Yabe M (2011) Preliminary list of the deep-sea fishes of the Sea of Japan. Bull Natl Mus Nat Sci, Ser A 37:35–62Google Scholar
  48. 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 53:357–368Google Scholar
  49. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Organi Divers Evol 12:335–337Google Scholar
  50. Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional, and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Res 11:914–921Google Scholar
  51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882Google Scholar
  52. Tyler PA (2002) Deep-sea eukaryote ecology of the semi-isolated basins off Japan. J Oceanog 58:333–341Google Scholar
  53. Ueno T (1970) Fauna Japonica, Cyclopteridae (Pisces). Acad Press Japan, TokyoGoogle Scholar
  54. Wang P (1999) Response of western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Mar Geol 156:5–39Google Scholar
  55. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philosoph Trans Royal Soc B 360:1847–1857Google Scholar

Copyright information

© The Ichthyological Society of Japan 2014

Authors and Affiliations

  • Yoshiaki Kai
    • 1
  • Duane E. Stevenson
    • 2
  • Yuji Ueda
    • 3
  • Tomonori Hamatsu
    • 4
  • Tetsuji Nakabo
    • 5
  1. 1.Maizuru Fisheries Research Station, Field Science Education and Research CenterKyoto UniversityMaizuruJapan
  2. 2.National Marine Fisheries Service, Alaska Fisheries Science Center, Resource Assessment and Conservation Engineering DivisionSeattleUSA
  3. 3.Japan Sea National Fisheries Research InstituteFisheries Research AgencyChuoJapan
  4. 4.Hokkaido National Fisheries Research InstituteFisheries Research AgencyKushiroJapan
  5. 5.The Kyoto University MuseumKyoto UniversitySakyoJapan

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