Marine Biology

, Volume 153, Issue 6, pp 1015–1022 | Cite as

Mitochondrial cytochrome b variation in sleeper sharks (Squaliformes: Somniosidae)

  • Brent William MurrayEmail author
  • John Y. Wang
  • Shih-Chu Yang
  • John D. Stevens
  • Aaron Fisk
  • Jörundur Svavarsson
Research Article


Sleeper sharks are a poorly studied group of deep-sea sharks. The subgenus, Somniosus, contains three morphologically similar species: S. microcephalus found in the Arctic and North Atlantic; S. pacificus in the North Pacific; and S. antarcticus in the Southern Ocean. These sharks have been reported mainly in temperate to polar waters and occasionally in subtropical locations. They have not been recorded in tropical waters. This study investigates the relationships among the accepted species of Somniosus through analysis of mitochondrial cytochrome b sequence variation. Seventy-five samples were examined from four sampling locations in the North Pacific, Southern Ocean and North Atlantic. Twenty-one haplotypes were found. A minimum spanning parsimony network separated these haplotypes into two divergent clades, an S. microcephalus and an S. pacificus/antarcticus clade, strongly supporting the distinction of S. microcephalus as a separate species from the Pacific sleeper shark species. Analysis of genetic structure within the S. pacificus/antarcticus clade (analysis of molecular variance, allele frequency comparisons, and a nested clade analysis) showed limited or no differences amongst three populations. Further examination of genetic variation at more variable mtDNA and nuclear markers is needed to examine the species status of S. pacificus and S. antarcticus.


Southern Ocean Shark Species Greenland Shark Hammerhead Shark Nest Clade Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We would like to thank Mark Thompson, UNBC, for technical assistance. For help with sample collections, would like to thank Ross Daley, CSIRO, (Antarctic samples), Kenneth J. Goldman, Virginia Institute of Marine Science, (Pacific samples), Hildibrandur Bjarnason (Iceland samples) and Mr. Chen (for Hualien samples). We also thank Dr. Lee-Shing Fang (National Museum of Marine Biology and Aquarium, Taiwan) for his support and encouragement. This work was supported by an NSERC Discovery Grant to BWM. This work complies with the current laws of Canada.


  1. Avise JC (2004) Molecular markers, natural history, and evolution. Sinauer Associates, Inc. 2nd edn. p 684Google Scholar
  2. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n populations by using a coalescent approach. PNAS 98:4563–4568PubMedCrossRefGoogle Scholar
  3. Benz GW, Hocking R, Kowunna AK Sr, Bullard SA, George JC (2004) A second species of Arctic shark: Pacific sleeper shark Somniosus pacificus from Point Hope, Alaska. Polar Biol 27:250–252CrossRefGoogle Scholar
  4. Bernardi G, Powers DA (1992) Molecular phylogeney of the prickly shark, Echinorhinus cookie, based on a nuclear (18S rRNA) and a mitochondrial (cytochrome b) gene. Mol Phylogenet Evol 2:161–167CrossRefGoogle Scholar
  5. Chakraborty R, Weiss KM (1991) Genetic variation of the mitochondrial DNA genome in American Indians is at mutation-drift equilibrium. Am J Hum Genet 86:497–506Google Scholar
  6. Chan RWK, Dixon PI, Pepperell JG, Reid DD (2003) Applications od DNA-based techniques for the identification of whaler sharks (Carcharhinus spp.) caught in protective beach meshing and by recreational fisheries off the coast of New South Wales. Fish Bull 101:910–914Google Scholar
  7. Chapman DD, Abercrombie DL, Douady CJ, Pikitch EK, Stanhope MJ, Shivji MS (2003) A streamlined, bi-organelle, multiplex PCR approach to species identification: application to global conservation and trade monitoring of the great white shark, Carcharondon carcharias. Conserv Genet 4:415–425CrossRefGoogle Scholar
  8. Clement M, Posado D, Crandall KA (2000) TCS: a computer program for estimating gene genologies. Mol Ecol 9:1757–1659CrossRefGoogle Scholar
  9. Compagno LJV (1984) FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of the shark species known to date. Part 1. Haxanchiformes to Lamniformes. FAO Fish Synop 4:1–249Google Scholar
  10. Duncan KM, Martin AP, Bowen BW, De Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251PubMedCrossRefGoogle Scholar
  11. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112PubMedCrossRefGoogle Scholar
  12. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  13. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and backgroud selection. Genetics 147:915–925PubMedGoogle Scholar
  14. Gardner MG, Ward RD (1998) Population structure of the Australian gummy shark (Mustelus antarcticus Guenther) inferred from allozymes, mitochondrial DNA and vertebrae counts. Mar Freshw Res 49:733–745CrossRefGoogle Scholar
  15. Heist EJ, Graves JE, Musick JA (1995) Population genetics of the sandbar shark (Carcharhinus plumbeus) in the Gulf of Mexico and Mid-Atlantic bight. Copeia 1995(3):555–562CrossRefGoogle Scholar
  16. Heist EJ, Musick JA, Graves JE (1996a) Mitochondrial DNA diversity and divergence among sharpnose sharks, Rhizoprionodon terraenovae, from the Gulf of Mexico and Mid-Atlantic bight. Fish Bull 94:664–668Google Scholar
  17. Heist EJ, Musick JA, Graves JE (1996b) Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Can J Fish Aquat Sci 53:583–588CrossRefGoogle Scholar
  18. Heist EJ, Gold JR (1999) Genetic identification of sharks in the U.S. Atlantic large coastal shark fishery. Fish Bull 97:53–61Google Scholar
  19. Herdendorf CE, Berra TM (1995) A Greenland shark from the wreck of the SS Central America at 2,200 meters. Trans Am Fish Soc 124:950–953CrossRefGoogle Scholar
  20. Hoelzel AR (2001) Shark fishing in fin soap. Conserv Genet 2:69–72CrossRefGoogle Scholar
  21. Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analysis of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923PubMedCrossRefGoogle Scholar
  22. Kitamura Y, Takemura A, Watabe S, Taniuchi T, Shimizu M (1996) Molecular phylogeny of the sharks and rays of superorder Squalea based on mitochondrial cytochrome b gene. Fish Sci 62:340–343Google Scholar
  23. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  24. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc Biol Sci 265:2257–2263CrossRefGoogle Scholar
  25. López JA, Ryburn JA, Fedrigo O, Naylor GJP (2006) Phylogeny of sharks of the family Triakidae (Carcharhiniformes) and its implication for the evolution of carchariniform placental viviparity. Mol Phylogenet Evol 40:50–60PubMedCrossRefGoogle Scholar
  26. Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution are slow in sharks compared to mammals. Nature 357:153–155PubMedCrossRefGoogle Scholar
  27. Naylor GJP, Martin AP, Mattison EG, Brown WM (1997) Interrelationships of Lamniform sharks: testing phylogenetic hypotheses with sequence data. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes, Academic PressGoogle Scholar
  28. Naylor GJP, Ryburn JA, Fedrigo O, López A (2005) Phylogenetic relationships among the major lineages of sharks and rays deduced from multiple genes. In: Hamlett W, Jamieson B (eds) Reproductive biology and phylogeny of Chondrichthyans (Sharks, skates, stingrays and chimaeras). Univ Queensland PressGoogle Scholar
  29. Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140PubMedCrossRefGoogle Scholar
  30. Pesole G, Gissi C, De Chirico A, Saccone C (1999) Nucleotide substitution rate of mammalian mitochondrial genomes. J Mol Evol 48:427–434PubMedCrossRefGoogle Scholar
  31. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  32. Sambrook J, Russell DW (2001) Molecular cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York, p 999Google Scholar
  33. Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  34. Schrey AW, Heist EJ (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Can J Fish Aquat Sci 60:670–675CrossRefGoogle Scholar
  35. Sezaki K, Begum RA, Wongrat P, Srivastava MP, SriKantha S, Kikuchi K, Ishihara H, Taniuchi T, Watabe S (1999) Molecular phylogeny of Asian freshwater and marine stingrays based on the DNA nucleotide and deduced amino acid sequences of the cytochrome b gene. Fish Sci 65:563–570Google Scholar
  36. Skomal GB, Benz GW (2004) Ultrasonic tracking of Greenland sharks, Somniosus microcephalus, under Arctic ice. Mar Biol 145:489–498CrossRefGoogle Scholar
  37. Stokesbury MJW, Harvey-Clark C, Gallant J, Block BA, Myers RA (2005) Movement and environmental preferences of Greenland sharks (Somniosus microcephalus) electronically tagged in the St. Lawrence Estuary, Canada. Mar Biol 148:159–165CrossRefGoogle Scholar
  38. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedGoogle Scholar
  39. Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465PubMedGoogle Scholar
  40. Templeman W (1963) Distribution of sharks in the Canadian Atlantic. Bull Fish Res Board Can No. 140Google Scholar
  41. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397PubMedCrossRefGoogle Scholar
  42. Wang JY, Yang S-C (2004) First records of Pacific sleeper sharks (Somniosus pacificus Bigelow and Schroeder, 1944) in the subtropical waters of eastern Taiwan. Bull Marine Sci 74:229–235Google Scholar
  43. Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276PubMedCrossRefGoogle Scholar
  44. Yano K, Stevens JD, Compagno LJV (2004) A review of the systematics of the sleeper shark genus Somniosus with a redescription of Somniosus (Somniosus) antarcticus and Somniosus (Rhinoscymnus) longus (Squaliformes: Somniosidea). Ichthyol Res 51:360–373CrossRefGoogle Scholar
  45. Zouros E (1979) Mutation rates, population sizes and amounts of electrophoretic variation of enzyme loci in natural populations. Genetics 92:623–646PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Brent William Murray
    • 1
    Email author
  • John Y. Wang
    • 2
    • 3
  • Shih-Chu Yang
    • 4
  • John D. Stevens
    • 5
  • Aaron Fisk
    • 6
  • Jörundur Svavarsson
    • 7
  1. 1.Ecosystem Science and Management ProgramUniversity of Northern British ColumbiaPrince GeorgeCanada
  2. 2.Formosacetus Research and Conservation GroupThornhillCanada
  3. 3.National Museum of Marine Biology & AquariumPingtung CountyTaiwan
  4. 4.Formosacetus Research and Conservation GroupHualien CountyTaiwan
  5. 5.CSIRO Marine & Atmospheric ResearchHobartAustralia
  6. 6.Great Lakes Institute for Environment ResearchUniversity of WindsorWindsorCanada
  7. 7.Institute of BiologyUniversity of IcelandReykjavikIceland

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