Abstract
The genetic structure of Patagonian toothfish populations in the Atlantic and western Indian Ocean Sectors of the Southern Ocean (SO) were analysed using partial sequences of the mitochondrial 12S rRNA gene and seven microsatellite loci. Both haplotype frequency data (F ST>0.906, P<0.01) and microsatellite genotype frequency data (F ST=0.0141–0.0338, P<0.05) indicated that populations of toothfish from around the Falkland Islands were genetically distinct from those at South Georgia (eastern Atlantic Sector SO), around Bouvet Island (western Atlantic Sector SO) and the Ob Seamount (western Indian Ocean Sector of the SO). Genetic differentiation between these populations is thought to result from hydrographic isolation, as the sites are separated by two, full-depth, ocean-fronts and topographic isolation, as samples are separated by deep water. The South Georgia, Bouvet and Ob Seamount samples were characterised by an identical haplotype. However, microsatellite genotype frequencies showed genetic differentiation between South Georgia samples and those obtained from around Bouvet Island and nearby seamounts (F ST=0.0037, P<0.05). These areas are separated by large geographic distance and water in excess of 3,000 m deep, below the distributional range of toothfish (<2,200 m). No significant genetic differentiation was detected between samples around Bouvet Island and the Ob Seamount although comparisons may have been influenced by low sample size. These localities are linked by topographic features, including both ridges and seamounts, that may act as oceanic “stepping stones” for migration between these populations. As for other species of deep-sea fish, Patagonian toothfish populations are genetically structured at the regional and sub-regional scales.
Similar content being viewed by others
References
Aboim MA, Menezes GM, Schlitt T, Rogers AD (2005) Genetic structure and history of populations of the deep-sea fish Helicolenus dactylopterus (Delaroche 1809) inferred from mtDNA sequence analysis. Mol Ecol 14:1343–1345
Agnew DJ, Heaps L, Jones C, Watson A, Berkieta K, Pearce J (1999) Depth distribution and spawning pattern of Dissostichus eleginoides at South Georgia. CCAMLR Sci 6:19–36
Appleyard SA, Ward RD, Williams R (2002) Population structure of the Patagonian toothfish around Heard, McDonald and Macquarie Islands. Antarct Sci 14(4):364–373
Appleyard SA, Williams R, Ward RD (2004) Population genetic structure of Patagonian toothfish in the West Indian Ocean Sector of the Southern Ocean. CCAMLR Sci 11:21–32
Arkhipkin A, Brickle P, Laptikhovsky V (2003) Variation in the diet of the Patagonian toothfish with size, depth and season around the Falkland Islands. J Fish Biol 63(2):428–441
Baker CS, Perry A, Chambers GK, Smith PJ (1995) Population variation in the mitochondrial cytochrome b gene of orange roughy Hoplostethus atlanticus and the hoki Macruronus novaezelandiae. Mar Biol 122:503–509
Chikov VN, Melnikov YS (1990) On the question of the fecundity of the Patagonian toothfish Dissostichus eleginoides in the region of Kerguelen Islands. J Ichthyol 30:122–125
Collins MA, Belchier M, Everson I (2003) Why the fuss about toothfish? Biologist 50(3):116–119
Creasey S, Rogers AD (1999) Population genetics of bathyal and abyssal organisms. Adv Mar Biol 35:1–151
Des Clers S, Nolan CP, Baranowski R, Pompert J (1996) Preliminary stock assessment of Patagonian toothfish longline fishery around the Falkland Islands. J Fish Biol 49(A):145–156
Evseenko SA, Kock K-H, Nevinsky MM (1995) Early life history of the Patagonian toothfish, Dissostichus eleginoides Smitt, 1898 in the Atlantic sector of the Southern Ocean. Antarct Sci 7(3):221–226
Fock HO, Zidowitz H (2004) Episodic recruitment to seamount populations: evidence from Zenopsis conchifer (Lowe, 1852) at the Great Meteor Seamount (subtropical North-east Atlantic). Arch Fish Mar Res 51(1–3):287–293
Glorioso PD (2000) Patagonian Shelf 3D tide and surge model. J Mar Syst 24:141–151
Goldsworthy SD, Lewis M, Williams R, He X, Young JW, van den Hoff J (2002) Diet of Patagonian toothfish (Dissostichus eleginoides) around Macquarie Island, South Pacific Ocean. Mar Freshw Res 53:49–57
Gon O, Heemstra PC (1990) Fishes of the Southern Ocean. J.L.B. Smith Institute of Ichthyology, Grahamstown, pp 462
Goudet J (1995) FSTAT version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486
Goudet J, Raymond M, de Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940
Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372
Hansen MM, Ruzzante DE, Nielsen EE, Bekkevold D, Mensberg KLD (2002) Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout (Salmo trutta) populations. Mol Ecol 11(12):2523–2535
Hoarau G, Borsa P (2000) Extensive gene flow within sibling species in the deep-sea fish Beryx splendens. C R Acad Sci III Vie 323:315–325
Horn PL (2002) Age and growth of Patagonian toothfish (Dissostichus eleginoides) and Antarctic toothfish (D. mawsoni) in waters from the New Zealand subantarctic to the Ross Sea, Antarctica. Fish Res 56:275–287
Kock K-H, Duhamel G, Hureau J-C (1985) Biology and status of exploited Antarctic stocks: a review. Biomass Sci Ser 6:143
Marlow TR, Agnew DJ, Purves MG, Everson I (2003) Movement and growth of tagged Dissostichus eleginoides around South Georgia and Shag Rocks (Subarea 48.3). CCAMLR Sci 10:101–112
Martin AP, Humphreys R, Palumbi SR (1992) Population genetic structure of the armourhead, Pseudopentaceros wheeleri, in the North Pacific Ocean: application of the polymerase chain reaction to fisheries populations. Can J Fish Aquat Sci 49:2368–2391
Meredith MP, Watkins JL, Murphy EJ, Ward P, Bone DG, Thorpe SE, Grant SD (2003a) Southern ACC front to the northeast of South Georgia: pathways, characteristics and fluxes. J Geophys Res 108(C5); doi 10.1029/2001JC001227, 2003
Meredith MP, Watkins JL, Murphy EJ, Cunningham NJ, Wood AG, Korb R, Whitehouse MJ, Thorpe SE, Vivier F (2003b) An anticyclonic circulation above the Northwest Georgia Rise, Southern Ocean. Geophys Res Letts 30(20):51–55
Milton DA, Shaklee JB (1987) Biochemical genetics and population structure of blue grenadier, Macruronus novaezelandiae (Hector) (Pisces: Merluccidae), from Australian waters. Aust J Mar Freshw Res 38:727–742
Møller PR, Nielsen JG, Fossen I (2003) Fish migration: Patagonian toothfish found off Greenland. Nature 421:599
Mullineaux LS, Mills SW (1997) A test of the larval retention hypothesis in seamount-generated flows. Deep Sea Res I 44(5):745–770
Nei M (1987) Molecular evolutionary genetics. Colombia University Press, New York, pp 512
North AW (2002) Larval and juvenile distribution and growth of Patagonian toothfish around South Georgia. Antarct Sci 14(1):25–31
Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR version 2.0. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu, 47pp
Pilling GM, Purves MG, Daw TM, Agnew DA, Xavier JC (2001) The stomach contents of Patagonian toothfish around South Georgia (South Atlantic). J Fish Biol 59:1370–1384
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Reilly A, Ward RD (1999) Microsatellite loci to determine stock structure of the Patagonian toothfish Dissostichus eleginoides. Mol Ecol 8(10):1753–1754
Rogers AD (2003) Molecular ecology and evolution of slope species. In: Wefer G, Billett D, Hebbeln D, Jørgensen B, Schlüter M, Van Weering T (eds) Ocean margin systems. Springer Verlag, Berlin, Heidelberg, pp 323–337
Ruzzante DE, Taggart CT, Cook D, Goddard SV (1997) Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: a test and evidence of temporal stability. Can J Fish Aquat Sci 54(11):2700–2708
Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN: a software for population genetics data analysis, version 2.00. Genetics and biometry laboratory, department of anthropology, University of Geneva, Switzerland
Sedberry GR, Carlin JL, Chapman RW, Eleby B (1996) Population structure in the pan-oceanic wreckfish, Polyprion americanus (Teleostei: Polyprionidae) as indicated by mtDNA variation. J Fish Biol 49(Suppl A):318–329
Shaw PW, Arkhipkin AI, Al-Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic polar front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13(11):3293–3304
Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417
Smith P, McVeagh M (2000) Allozyme and microsatellite DNA markers of toothfish population structure in the Southern Ocean. J Fish Biol 57(Suppl A):72–83
Smith PJ, Francis RICC (1982) A glucosephosphate isomerase polymorphism in New Zealand ling Genypterus blacodes. Comp Biochem Physiol 73B:451–455
Smith PJ, Gaffney PM, Purves M (2001) Genetic markers for identification of Patagonian toothfish and Antarctic toothfish. J Fish Biol 58:1190–1194
Smith PJ, McVeagh SM, Ede A (1996) Genetically isolated stocks of orange roughy (Hoplostethus atlanticus), but not of hoki (Macruronus novaezealandiae), in the Tasman Sea and Southwest Pacific Ocean around New Zealand. Mar Biol 125:783–793
Smith PJ, Paulin CD (2003) Genetic and morphological evidence for a single species of pink ling (Genypterus blacodes) in New Zealand waters. NZ J Mar Freshw Res 37:183–194
Stockley B, Menezes G, Pinho M, Rogers AD (2005) Genetic population structure in the black-spot sea bream (Pagellus bogaraveo Brünnich, 1768) from the NE Atlantic. Mar Biol 146(4):793–804
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
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 25:4876–4882
Thorpe SE, Stevens DP, Heywood KJ (2005) Comparison of two time-variant forced eddy-permitting global ocean circulation models with hydrography of the Scotia Sea. Ocean Model 9:105–132
Tuck GN, de la Mare WK, Hearn WS, Williams R, Smith ADM, He X, Constable A (2003) An exact time of release and recapture stock assessment model with an application to Macquarie Island Patagonian toothfish (Dissostichus eleginoides). Fish Res 63:179–191
Ward RD, Elliot NG, Grewe PM, Last PR, Lowry PS, Innes BH, Yearsley GK (1998) Allozyme and mitochondrial DNA variation in three species of oreos (Teleostei: Oreosomatidae) from Australian waters. NZ J Mar Freshw Res 32:233–245
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Williams R, Tuck GN, Constable AJ, Lamb T (2002) Movement, growth and available abundance to the fishery of Dissostichus eleginoides Smitt, 1898 at Heard Island, derived from tagging experiments. CCAMLR Sci 9:33–48
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
Wright S (1978) Evolution and the genetics of populations, vol 4. University of Chicago Press, Chicago and London, pp 590
Xavier JC, Rodhouse PG, Purves MG, Daw TM, Arata J, Pilling GM (2002) Distribution of cephalopods recorded in the diet of the Patagonian toothfish (Dissostichus eleginoides) around South Georgia. Polar Biol 25:323–330
Acknowledgements
We thank Dr Eduardo Balguerías for sampling and provision of toothfish samples from Speiss, Meteor and Ob Seamounts and Bouvet Island. Dr Paul Brickle provided toothfish samples from the Falklands Islands whilst samples from the Shag Rocks/South Georgia regions were provided by scientific observers working on commercial longline vessels and from a survey conducted by the FRV “Dorada”. Simon Morley was funded by the Government of South Georgia and South Sandwich Islands (GSGSSI), through the South Georgia Project. Kester Jarvis received an Undergraduate Research Bursary (Ref: URB/01449/G) from the Nuffield Foundation for a summer internship at British Antarctic Survey, Cambridge. We also acknowledge Dr Michael Meredith for comments on the oceanographic discussion in the paper, Dr Tony North and Dr Martin Collins for comments on toothfish biology, and Prof. Paul Rodhouse and Prof Christopher Rapley for provision of facilities at British Antarctic Survey, Cambridge.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J.P. Thorpe, Port Erin
Rights and permissions
About this article
Cite this article
Rogers, A.D., Morley, S., Fitzcharles, E. et al. Genetic structure of Patagonian toothfish (Dissostichus eleginoides) populations on the Patagonian Shelf and Atlantic and western Indian Ocean Sectors of the Southern Ocean. Mar Biol 149, 915–924 (2006). https://doi.org/10.1007/s00227-006-0256-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-006-0256-x