Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-19T13:31:52.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary history told by mitochondrial markers of large teleost deep-sea predators of family Anoplopomatidae Jordan & Gilbert 1883, endemic to the North Pacific

Published online by Cambridge University Press:  05 September 2019

Svetlana Y. Orlova ,
Dimitry M. Schepetov Open the ORCID record for Dimitry M. Schepetov [Opens in a new window] ,
Nikolai S. Mugue ,
Maria A. Smirnova ,
Hiroshi Senou ,
Aleksei A. Baitaliuk  and
Alexei M. Orlov
Svetlana Y. Orlova
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia
Dimitry M. Schepetov*
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia Koltzov Institute of Developmental Biology of Russian Academy of Sciences, Moscow, Russia National Research University ‘Moscow Power Engineering Institute’, Moscow, Russia National Research University Higher School of Economics, Moscow, Russia
Nikolai S. Mugue
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia Koltzov Institute of Developmental Biology of Russian Academy of Sciences, Moscow, Russia
Maria A. Smirnova
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia
Hiroshi Senou
Affiliation:
Kanagawa Prefectural Museum of Natural History, Odawara, Japan
Aleksei A. Baitaliuk
Affiliation:
Pacific Fisheries Research Center, Vladivostok, Russia
Alexei M. Orlov
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences, Moscow, Russia Dagestan State University, Makhachkala, Russia Tomsk State University, Tomsk, Russia
*
Author for correspondence: Dimitry M. Schepetov, E-mail: d.schepetov@idbras.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

We propose three calibration scenarios of to date contemporary divergence of Anoplopomatidae (skilfish Erilepis zonifer and sablefish Anoplopoma fimbria) for a data set of two mtDNA loci (СOI and Control Region). The first scenario is based upon a fossil record and the second and third ones upon major palaeogeological events 3.5 and 15 Mya. Estimated evolution speeds indicate that COI evolves faster in the skilfish mitochondrial genome. There is also evidence of skilfish going through a bottleneck event limiting its genetic diversity in the relatively recent past near Japan. Sablefish had two refugia on both sides of the Pacific Ocean. The contemporary haplotype divergence was formed ~450 thousand years ago during an ice age in the Pleistocene and contemporary populations display no apparent geographic differentiation.

Keywords

COIControl RegionNorth Pacificphylogeographysablefish Anoplopoma fimbriaskilfish Erilepis zonifer
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 7 , November 2019 , pp. 1683 - 1691
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andriashev, AP (1939) On the amphipacific (Japan-Oregonian) distribution of sea-fauna in the northern part of the Pacific Ocean. Zoologicheskii Zhurnal 17, 181–195.Google Scholar
Beamish, RJ and McFarlane, GA (1988) Resident and dispersal behavior of adult sablefish (Anoplopoma fimbria) in the slope waters off Canada's west coast. Canadian Journal of Fisheries and Aquatic Sciences 45, 152–164.Google Scholar
Beamish, RJ and McFarlane, GA (2000) Reevaluation of the interpretation of annuli from otoliths of a long-lived fish, Anoplopoma fimbria. Fisheries Research 46, 105–111.Google Scholar
Bernardi, G (2005) Phylogeography and demography of sympatric sister surfperch species, Embiotoca jacksoni and E. lateralis along the California coast: historical vs ecological factors. Evolution 59, 386–394.Google Scholar
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, CH, Xie, D and Drummond, AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.Google Scholar
Briggs, JC (1970) A faunal history of the north Atlantic Ocean. Systematic Zoology 19, 19–34.Google Scholar
Briggs, JC (1974) Marine Zoogeography. New York, NY: McGraw-Hill.Google Scholar
Briggs, JC (1995) Global Biogeography. Amsterdam: Elsevier Science.Google Scholar
Briggs, JC (2003) Marine centres of origin as evolutionary engines. Journal of Biogeography 30, 1–18.Google Scholar
Brunner, PC, Douglas, MR, Osinov, AG, Wilson, CC and Bernatchez, L (2001) Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evolution 55, 573–586.Google Scholar
Clemens, WA and Wilby, GV (1961) Fishes of the Pacific Coast of Canada. Fisheries Research Board of Canada Bulletin 68, 1–443.Google Scholar
Coates, AG and Stallard, RF (2013) How old is the Isthmus of Panama? Bulletin of Marine Science 89, 801–813.Google Scholar
Donaldson, KA and Wilson, RR Jr (1999) Amphi-panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Molecular Phylogenetics and Evolution 13, 208–213.Google Scholar
Drummond, AJ, Ho, SYW, Phillips, MJ and Rambaut, A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.Google Scholar
Drummond, AJ, Ashton, B, Buxton, S, Cheung, M, Cooper, A, Duran, C and Moir, R (2011) Geneious v5.4. Available at http://www.geneious.com/.Google Scholar
Dudnik, YI, Kodolovm, LS and Polutovm, VI (1998) On the distribution and reproduction of Anoplopoma fimbria off the Kuril Islands and Kamchatka. Journal of Ichthyology 38, 12–17.Google Scholar
Eschmeyer, WN, Herald, ES and Hamman, H (1983) A Field Guide to Pacific Coast Fishes. Boston, MA: Houghton Mifflin Co.Google Scholar
Fierstine, HL, Huddleston, RW and Takeuchi, GT (2012) Catalog of the Neogene bony fishes of California. A systematic inventory of all published accounts. Occasional Papers of the California Academy of Sciences 159, 1–206.Google Scholar
Friesen, EN, Balfry, SK, Skura, BJ, Ikonomu, MG and Higgs, DA (2013) Evaluation of cold pressed flaxseed oil as an alternative dietary lipid source for juvenile sablefish (Anoplopoma fimbria). Aquaculture Research 44, 182–199.Google Scholar
Froese, R and Pauly, D (eds) (2018) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org.Google Scholar
Gladenkov, AY, Oleinik, AE, Marincovich, L and Barinov, KB (2002) A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology 183, 321–328.Google Scholar
Habib, KA, Jeong, D, Myoung, JG, Kim, MS, Jang, YS, Shim, JS and Lee, YH (2011) Population genetic structure and demographic history of the fat greenling Hexagrammos otakii. Biochemical Systematics and Ecology 33, 413–423.Google Scholar
Hart, JL (1973) Pacific fishes of Canada. Fisheries Research Board of Canada Bulletin 180, 1–740.Google Scholar
Haug, GH and Tiedemann, R (1998) Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393, 673–676.Google Scholar
Haug, GH, Tiedemann, R, Zahn, R and Ravelo, AC (2001) Role of Panama uplift on oceanic freshwater balance. Geology 29, 207–210.Google Scholar
Hopkins, DM, Rowland, RW and Patton, WW (1972) Middle Pleistocene mollusks from St. Lawrence Island and their significance for the paleo-oceanography of the Bering Sea. Quaternary Research 2, 119–134.Google Scholar
Hunter, JR, Macewicz, BJ and Kimbrell, CA (1989) Fecundity and other aspects of the reproduction of sablefish, Anoplopoma fimbria, in central California waters. CalCOFI Reports 30, 61–72.Google Scholar
Humphreys, RL and Tagami, DT (1986) Review and current status of research and ecology of the genus Pseudopentaceros. NOAA Technical Report NMFS 43, 55–62.Google Scholar
Ivanova, NV, Zelmak, TS, Hanner, RH and Hebert, PDN (2007) Universal primer cocktails for fish DNA barcoding. Molecular Ecology Resources 7, 544–548.Google Scholar
Jasonowicz, AJ, Goetz, FW, Goetz, GW and Nichols, KM (2016) Love the one you're with: genomic evidence of panmixia in the sablefish (Anoplopoma fimbria). Canadian Journal of Fisheries and Aquatic Sciences 74, 377–387.Google Scholar
Jordan, DS and Gilbert, JZ (1919) Fossil Fishes of Southern California. Redwood City, CA: Stanford University Press.Google Scholar
Kameo, K and Sato, T (2000) Biogeography of Neogene calcareous nannofossils in the Caribbean and the eastern equatorial Pacific – floral response to the emergence of the Isthmus of Panama. Marine Micropaleontology 39, 201–218.Google Scholar
Katafuchi, H and Nakabo, T (2007) Revision of the East Asian genus Ditrema (Embiotocidae), with description of a new subspecies. Ichthyological Research 54, 350–366.Google Scholar
Keigwin, L (1982) Isotopic paleooceanography of the Caribbean and East Pacific: role of Panama uplift in late Neogene time. Science 217, 350–353.Google Scholar
Kim Sen Tok, (2000) On the occurrence of Anoplopoma fimbria (Anoplopomatidae) off the southeastern coast of Sakhalin Island. Journal of Ichthyology 40, 709–710.Google Scholar
Knowlton, N and Weigt, LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London, Part B 265, 2257–2263.Google Scholar
Kodolov, LS (1986) Sablefish. In Vinogradov, MV, Parin, NV and Shuntov, VP (eds) Biological Resources of the Pacific Ocean. Moscow: Nauka, pp. 328–340.Google Scholar
Lea, RN (2013) Record of the Kamchatka Flounder, Atheresthes evermanni, in California waters. Northwestern Naturalist 94, 244–246.Google Scholar
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.Google Scholar
Leigh, EG, O'Dea, A and Vermeij, GJ (2014) Historical biogeography of the Isthmus of Panama. Biological Reviews 89, 148–172.Google Scholar
Lindberg, GU and Krasyukova, ZV (1987) Fishes of the Sea of Japan and Adjacent Areas of Okhotsk and Yellow Seas. Pt. 5. Leningrad: Nauka.Google Scholar
Love, MS, Yoklavich, M and Thorsteinson, L (2002) The Rockfishes of the Northeast Pacific. Berkeley, CA: University of California Press.Google Scholar
Lyle, MW, Barron, JA, Bralower, TJ, Huber, M, Lyle, AO, Ravelo, AC, Kenerson Rea, D and Wilson, PA (2008) Pacific Ocean and Cenozoic evolution of climate. Reviews of Geophysics 46, RG2002.Google Scholar
Marincovich, L and Gladenkov, AY (1999) Evidence for an early opening of the Bering Strait. Nature 397, 149–151.Google Scholar
Marko, PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Molecular Biology and Evolution 19, 2005–2021.Google Scholar
Martin, AP, Naylor, GJP and Palumbi, SR (1992) Population genetic structure of the armorhead Pseudopentaceros wheeleri, in the North Pacific ocean: application of the polymerase chain reaction to fisheries problems. Canadian Journal of Fisheries and Aquatic Sciences 49, 2386–2391.Google Scholar
Mason, JC, Beamish, RJ and McFarlane, GA (1983) Sexual maturity, fecundity, spawning, and early life history of sablefish (Anoplopoma fimbria) off the Pacific coast of Canada. Canadian Journal of Fisheries and Aquatic Sciences 40, 2126–2134.Google Scholar
Matthiessen, J, Knies, J, Vogt, C and Stein, R (2009) Pliocene palaeoceanography of the Arctic Ocean and subarctic seas. Philosophical Transactions of the Royal Society of London A 367, 21–48.Google Scholar
McCraney, WT, Saski, CA and Guyon, JR (2012) Isolation and characterization of 12 microsatellites for the commercially important sablefish, Anoplopoma fimbria. Conservation Genetic Resources 4, 415–417.Google Scholar
McFarlane, GA and Beamish, RJ (1995) Validation of the otolith x-section method of age determination for sablefish using OTC. In Secor, DH, Campana, SE and Dean, JM (eds), Recent Developments in Fish Otolith Research. Columbia, SC: University of South Carolina Press, pp. 319–330.Google Scholar
Millar, CI (2012) Geologic, climatic, and vegetation history of California. In Baldwin, BG, Goldman, DH, Keil, DJ, Patterson, R, Rosatti, T and Wilken, DH (eds) Vascular Plants of California. Berkeley, CA: University of California Press, pp. 49–68.Google Scholar
Mitani, I, Kamei, M and Shimizu, T (1986) Some aspects of biology and fisheries of skilfish (Erilepis zonifer (Lockington)) off Japan. Kamisuikenhou 7, 23–27.Google Scholar
Montes, C, Cardona, A, Jaramillo, C, Pardo, A, Silva, JC, Valencia, V and Niño, H (2015) Middle Miocene closure of the Central American seaway. Science 348, 226–229.Google Scholar
Moore, DG (1964) Acoustic-reflection reconnaissance of continental shelves – Eastern Bering and Chukchi Seas. In Miller, RL (ed.), Papers in Marine Geology. London: Macmillan, pp. 319–362.Google Scholar
Nof, D and Van Gorder, S (2003) Did an open Panama Isthmus correspond to an invasion of Pacific water into the Atlantic? Journal of Physical Oceanography 33, 1324–1336.Google Scholar
Novikov, NP (1969) Sablefish [Anoplopoma fimbria (Pall.)] and arrow-tooth flounder [Atheresthes stomias (Jord. et Gilb.)] in the Sea of Okhotsk. Zoologicheskii Zhurnal 48, 610–611.Google Scholar
Novikov, NP (1974) Commercial Fishes of Continental Slope of the North Pacific Ocean. Moscow: Pishchevaya Promyshlennost.Google Scholar
Novikov, NP (1994) New captures of sablefish Anoplopoma fimbria in the Sea of Okhotsk. Voprosy Ikhtiologii 34, 843–845.Google Scholar
Okamoto, M, Watanabe, Y and Asahida, T (2010) A larva of the skilfish, Erilepis zonifer (Actinopterygii: Scorpaeniformes: Anoplopomatidae), from off Northeastern Japan. Species Diversity 15, 125–130.Google Scholar
Okonechnikov, K, Golosova, O and Fursov, M (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28, 1166–1167.Google Scholar
Orlov, AM (1999) New northwest Pacific record of the Pacific black scabbardfish Aphanopus arigato (Trichiuridae, Perciformes) in the vicinity of southeastern Kamchatka. Acta Ichthyologica et Piscatoria 29, 3–11.Google Scholar
Orlov, AM and Biryukov, IA (2005) First report of sablefish in spawning condition off the coast of Kamchatka and the Kuril Islands. ICES Journal of Marine Science 62, 1016–1020.Google Scholar
Orlov, AM and Tokranov, AM (2003) Skilfish Erilepis zonifer (Anoplopomatidae): history of study and new data on distribution and biology. Izvestiya TINRO 135, 3–29.Google Scholar
Orlov, AM and Tokranov, AM (2006) Spatial distribution and dynamics of catches of Sebastes glaucus, S. iracundus and S. polyspinis in Pacific waters off the Kuril Islands and Kamchatka. Journal of Ichthyology 46, 625–639.Google Scholar
Orlov, AM, Tokranov, AM and Megrey, BA (2012) A review of the knowledge related to the nomenclature, etymology, morphology, distribution, and biological characteristics of the skilfish, Erilepis zonifer (Anoplopomatidae), in the North Pacific Ocean. In Bailey, DR and Howard, SE (eds), Deep-Sea: Marine Biology, Geology, and Human Impact. Hauppauge, NY: Nova Science Publishers, pp. 63–100.Google Scholar
Orlova, SY, Orlov, AM, Volkov, AA and Novikov, RN (2014) Micro-evolutionary processes in sablefish Anoplopoma fimbria, based on polymorphism of the two sites of mitochondrial DNA. Doklady Biochemistry and Biophysics 458, 172–176.Google Scholar
Orozco-Ruiz, AM, Galván-Tirado, C, Orlova, SY, Orlov, AM and García-De León, FJ (2018) Microsatellite loci obtained by next generation sequencing on the sablefish (Anoplopoma fimbria). Molecular Biology Reports 45, 1523–1526.Google Scholar
Parin, NV (1988) Fishes of the High Seas. Moscow: Nauka.Google Scholar
Rambaut, A and Drummond, A (2008) FigTree: Tree figure drawing tool, version 1.2.2. University of Edinburgh, Edinburgh.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.Google Scholar
Romine, K and Lombari, G (1985) Evolution of Pacific circulation in the Miocene: radiolarian evidence from DSDP Site 289. Geological Society of America Memoirs 163, 273–290.Google Scholar
Safran, P and Omori, M (1990) Some ecological observations on fishes associated with drifting seaweed off Tohoku coast, Japan. Marine Biology 105, 395–402.Google Scholar
Sanderson, MJ (2003) R8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302.Google Scholar
Sasaki, T (1985) Studies on the sablefish resources of the North Pacific Ocean. Bulletin of the Far Seas Fisheries Research Laboratory 22, 1–107.Google Scholar
Shenker, JM and Olla, BL (1986) Laboratory feeding and growth of juvenile sablefish, Anoplopoma fimbria. Canadian Journal of Fisheries and Aquatic Sciences 43, 930–937.Google Scholar
Silva, WA Jr, Costa, MC, Valente, V, Sousa, JF, Paçó-Larson, ML, Espreafico, EM, Camargo, SS, Monteiro, E, Holanda, AJ, Zago, MA, Simpson, AJ and Dias Neto, E (2001) PCR template preparation for capillary DNA sequencing. BioTechniques 30, 537, 540–542.Google Scholar
Shinohara, G (1994) Comparative morphology and phylogeny of the suborder Hexagrammoidei and related taxa (Pisces: Scorpaeniformes). Memoirs of the Faculty of Fisheries – Hokkaido University (Japan) 40, 1–97.Google Scholar
Sogard, SM and Olla, BL (2001) Growth and behavioral responses to elevated temperatures by juvenile sablefish Anoplopoma fimbria and the interactive role of food availability. Marine Ecology Progress Series 217, 121–134.Google Scholar
Starr, RM, O'Connell, V and Ralston, S (2004) Movements of lingcod (Ophiodon elongatus) in southeast Alaska: potential for increased conservation and yield from marine reserves. Canadian Journal of Fisheries and Aquatic Sciences 61, 1083–1094.Google Scholar
Tokranov, AM (2002) On occurrence of juveniles of sablefish Anoplopoma fimbria (Pallas) (Anoplopomatidae) in waters off Kamchatka. Okeanologiya 42, 124–126.Google Scholar
Tokranov, AM and Orlov, AM (2007) The features of distribution and several biological traits of sablefish Anoplopoma fimbria in the Pacific Ocean waters of Southeast Kamchatka and the Northern Kuril Islands. Research of Aquatic Biological Resources of Kamchatka and the Northwestern Pacific 9, 191–204.Google Scholar
Tokranov, AM, Orlov, AM and Sheiko, BA (2005) Commercial Fishes of Kamchatka Continental Slope. Petropavlovsk-Kamchatsky: Kamchatpress.Google Scholar
Tripp-Valdez, MA, García-de-León, FJ, Espinosa-Pérez, H and Ruiz-Campos, G (2012) Population structure of sablefish Anoplopoma fimbria using genetic variability and geometric morphometric analysis. Journal of Applied Ichthyology 28, 516–523.Google Scholar
Ward, RD, Zemlak, TS, Innes, BH, Last, PR and Hebert, PDN (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B 360, 1847–1857.Google Scholar
Zolotov, OG and Spirin, IY (2012) On the fishery and abundance of skilfish (Erilepis zonifer) at the Emperor Seamounts (North-West Pacific). Izvestiya TINRO 168, 79–88. [In Russian]Google Scholar
Zolotov, OG, Spirin, IY and Zudina, SM (2014) New data on the range, biology, and abundance of skilfish Erilepis zonifer (Anoplopomatidae). Journal of Ichthyology 54, 251–265.Google Scholar