Advertisement

Marine Biology

, Volume 116, Issue 4, pp 593–602 | Cite as

Genetic evidence of population heterogeneity and cryptic speciation in the ommastrephid squid Martialia hyadesi from the Patagonian Shelf and Antarctic Polar Frontal Zone

  • A. S. Brierley
  • P. G. Rodhouse
  • J. P. Thorpe
  • M. R. Clarke
Article

Abstract

Horizontal starch gel electrophoresis was used to investigate levels of genetic differentiation between four samples of the nominate squid species Martialia hyadesi Rochbrune and Mabille, 1889, obtained from regions of the Patagonian Shelf and Antarctic Polar Fron-tal Zone over 1000 km apart. M. hyadesi is an ecologically important South Atlantic ommastrephid squid and it is probable that, in the future, fishing effort will be increasingly directed towards this species. Details regarding the population structure of the species are therefore required. In comparison with the other three samples of M. hyadesi, one of the samples from the Patagonian Shelf (PAT 89II) exhibited fixed allelic differences at 16 of the 39 enzyme loci which were resolved (genetic identity, I=0.51). This high level of genetic differentiation contradicts the apparent morphological similarity between samples, indicating the presence of a cryptic or sibling congeneric species. Deviations from Hardy-Weinberg equilibrium and significant differences in allele distribution were also detected within and between the other three putative M. hyadesi samples, suggesting that the species fails to maintain effective panmixia across its geographical range. The occurrence of both temporal (1986 cf. 1989) and geographic structuring within the species complex is consequently indicated, caused possibly by an overlap of reproductively isolated stocks (stock mixing) outside their respective breeding areas. Low levels of genetic variability were detected throughout the samples examined, estimates of average heterozygosity per locus within the two species detected being in the order of 0.01 and 0.002. These values are discussed in relation to levels of genetic variability reported for other squid species, and in comparison with values typically expected for marine invertebrates.

Keywords

Fishing Genetic Differentiation Cryptic Speciation Fishing Effort Genetic Identity 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Allendorf, F. W., Ryman, N., Utter, F. M. (1987). Genetics and fishery management. Past, present and future. In: Ryman, N., Utter, F. M. (eds.). Population genetics and fishery management. University of Washington Press, Seattle, p. 1–18Google Scholar
  2. Ally, J. R. R., Keck, S. C. (1978). A biochemical genetic population structure study of market squid, Loligo opalescens, along the California coast. Calif. Fish Game Fish Bull. 169:113–121Google Scholar
  3. Amaratunga, T. (1987). Population biology. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol. 2. Comparative reviews. Academic Press, London, p. 239–252Google Scholar
  4. Anonymous. (1989). Falkland Islands interim conservation and management zone. Fisheries report '87/88. Falkland Islands Government, Port Stanley, Falkland IslandsGoogle Scholar
  5. Arnold, C. P. (1979). Squid, a review of their biology and fisheries. Lab. Leafl. Minist. Agric. Fish. Fd Direct. Fish. Res., Lowestoft 48:1–37Google Scholar
  6. Augustyn, C. J., Grant, W. S. (1988). Biochemical and morphological systematics of Loligo vulgaris vulgaris Lamarck and Loligo vulgaris reynaudii D'Orbigny nov. comb. (Cephalopoda: Myopsida). Malacologia 29:215–233Google Scholar
  7. Avise, J. C. (1974). Systematic value of electrophoretic data. Syst. Zool. 23: 465–481Google Scholar
  8. Ayala, F. J. (1983). Enzymes as taxonomic characters. In: Oxford, G. S., Rollinson, D. (eds.) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, p. 3–26Google Scholar
  9. Bonnell, M. L., Selander, R. K. (1974). Elephant seals, genetic variation and near extinction. Science, N.Y. 184:908–909Google Scholar
  10. Boyer, S. H., Fainer, D. C., Naughton, M. A. (1963). Myoglobin: inherited structural variation in man. Science, N.Y. 140:1228–1231Google Scholar
  11. Brewer, G. J. (1970). An introduction to isozyme technique. Academic Press, New YorkGoogle Scholar
  12. Brierley, A. S. (1992). Aspects of genetic diversity and population structure in squid. Unpublished thesis. University of Liverpool, Port Erin, Isle of ManGoogle Scholar
  13. Brierley, A. S., Thorpe, J. P., Clarke, M. R., Martins, H. R. (1993). A preliminary biochemical genetic investigation of the population structure of Loligo forbesi Steenstrup, 1856 from the U.K. and the Azores. In: Okutani, T. (ed.) Recent advances in cephalopod fishery biology. Tokai University Press, Shimizu, Japan (in press)Google Scholar
  14. Carvalho, G. R., Loney, K. H. (1989). Biochemical genetic studies on the Patagonian squid Loligo gahi d'Orbigny. I. Electrophoretic study of genetic variability. J. exp. mar. Biol. Ecol. 126:231–241Google Scholar
  15. Carvalho, G. R., Pitcher, T. J. (1989). Biochemical genetic studies on the Patagonian squid Loligo gahi d'Orbigny. II. Population structures in Falkland waters using morphometrics and life history data. J. exp. mar. Biol. Ecol. 126:243–258Google Scholar
  16. Carvalho, G. R., Thompson, A., Stoner, A. L. (1992). Genetic diversity and population differentiation in the shortfin squid (Illex argentinus) in the south-west Atlantic. J. exp. mar. Biol. Ecol. 158:105–121Google Scholar
  17. Chakraborty, R., Fuerst, P. A., Nei, M. (1978). Statistical studies on protein polymorphism in natural populations II. Gene differentiation between populations. Genetics Austin, Tex. 88:367–390Google Scholar
  18. Christofferson, J. P., Foss, A., Lambert, W. E., Welge, B. (1978). An electrophoretic study of select proteins from the market squid, Loligo opalescens, along the California coast. Calif. Fish Game Fish Bull. 169:123–133Google Scholar
  19. Clarke, M. R. (1966). A review of the systematics and ecology of oecanic squids. Adv. mar. Biol. 4: 91–300Google Scholar
  20. Csirke, J. (1987). The Patagonian fishery resources and the offshore fisheries in the South-West Atlantic. F.A.O. Fish. tech. Pap. 286: 1–75Google Scholar
  21. Dando, P. R., Storey, K. B., Hochachka, P. W., Storey, J. M. (1981). Multiple dehydrogenases in marine molluscs: electrophoretic analysis of alanopine dehydrogenase, strombine dehydrogenase, octopine dehydrogenase and lactate dehydrogenase. Mar. Biol. Lett. 2:249–257Google Scholar
  22. Everhart, W. H., Eipper, A. W., Young, W. D. (1975). Principles of fishery science. Cornell University Press, Ithaca, N.Y.Google Scholar
  23. Fildes, R. A., Harris, H. (1966). Genetically determined variation of adenylate kinase in man. Nature, London. 209: 261–263Google Scholar
  24. Garthwaite, R. L., Berg, C. J., Jr., Harrigan, J. (1989). Population genetics of the common squid Loligo pealei LeSeur, 1821, from Cape Cod to Cape Hatteras. Biol. Bull. mar. biol. Lab., Woods Hole 177:287–294Google Scholar
  25. Harris, H., Hopkinson, D. A. (1977). Handbook of enzyme electrophoresis in human genetics. North Holland Publishing Co., AmsterdamGoogle Scholar
  26. Hartl, D. L., Clark, A. G. (1989). Principles of population genetics. 2nd ed. Sinauer Associates, Sunderland, Mass.Google Scholar
  27. Ihssen, P. E., Booke, H. E., Casselman, J. M., McGlade, J. M., Payne, N. R., Utter, F. M. (1981). Stock identification, materials and methods. Can. J. Fish. aquat. Sciences 38:1838–1855Google Scholar
  28. Jeremiah, S. J., Povey, S., Burley, M. W., Kietly, C., Lee, M., Spowart, G., Carney, G., Cook, P. J. L. (1982). Mapping studies on human mitochondrial glutamate oxaloacetate transaminase. Ann. hum. Genet. 46:145–152Google Scholar
  29. Katoh, M., Foltz, D. W. (1988). Determination of null allele frequency at an allozyme locus in a natural oyster population. National Shellfisheries Association Annual Meeting 203. National Shellfisheries Association, New Orleans, LouisianaGoogle Scholar
  30. Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press, LondonGoogle Scholar
  31. Koehn, R. K., Hilbish, T. J. (1987). The adaptive importance of genetic variation. Am. Scient. 75:134–141Google Scholar
  32. Levy, J. A., Haimovici, M., Conceicao, M. (1988). Genetic evidence for two species to the genus Eledone (Cephalopoda: Octopodidae) in South Brazil. Comp. Biochem. Physiol. 90B:275–277Google Scholar
  33. Lipinski, M. (1979). Universal maturity scale for the commercially important squids (Cephalopoda: Teuthoidea). The results of maturity classification of the Illex illecebrosus (LeSeur, 1821) populations for the years 1973–77. Res. Docums int. Commn NW. Atlant. Fish. (ICNAF) 79/11/38:1–40Google Scholar
  34. Mallet, A. L., Haley, L. E. (1983). Effects of inbreeding on larval and spat performance in the American oyster. Aquaculture, Amsterdam 33:229–235Google Scholar
  35. Maynard Smith, J. (1989). Evolutionary genetics. Oxford University Press, OxfordGoogle Scholar
  36. Natsukari, Y., Nishiyama, Y., Nakanishi, Y. (1986). A preliminary study on the isozymes of the loliginid squid Photololigo edulis (Hoyle, 1885). Rep. coop. Invest. Shiro-ika Loligo edulis Inhab. W Japan. Sea 2:145–151. (Cited after Carvalho and Loney 1989)Google Scholar
  37. Nei, M. (1972). Genetic distance between populations. Am. Nat. 106:283–292Google Scholar
  38. Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  39. Nesis, K. N. (1987). Cephalopods of the world. T.F.H. Publications Inc., Neptune, City, N.J.Google Scholar
  40. Nevo, E. (1978). Genetic variation in natural populations: patterns and theory. Theor. Popul. Biol. 13:121–177Google Scholar
  41. Nevo, E. (1983). Adaptive significance of protein polymorphism. In: Oxford, G. S., Rollinson, D. (eds.) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, p. 239–282Google Scholar
  42. Nevo, E., Beiles, A., Ben-Schlomo, R. (1984). The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: Mani, G. S. (ed.) Evolutionary dynamics of genetic diversity, Lecture notes in biomathematics. Vol. 53. Springer-Verlag, Heidelberg, p. 13–213Google Scholar
  43. O'Brien, S. J., Wildt, D. E., Bush, M., Caro, T. M., FitzGibbon, C., Aggundey, I., Leakey, R. E. (1987). East African cheetahs: evidence for two population bottlenecks. Proc. natn. Acad. Sci. U.S.A. 84:508–511Google Scholar
  44. Patterson, K. (1987). Fishy events in the Falklands. New Scient. 1562:44–48Google Scholar
  45. Poulik, M. D. (1957). Starch gel electrophoresis in a discontinuous system of buffers. Nature, Lond. 180:1477–1479Google Scholar
  46. Rathjen, W. F., Voss, G. L. (1987). The cephalopod fisheries: a review. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol. 2. Academic Press, London, p. 253–275Google Scholar
  47. Richardson, B. J. (1983) Final report on the genetic analysis of the arrow squid from the waters around south eastern Australia. Fisheries Development Trust Account Programme, Sydney (Unpublished report)Google Scholar
  48. Richardson, B. J., Baverstock, P. R., Adams, M. (1986). Allozyme electrophoresis — a handbook for animal systematics and population studies. Academic Press, SydneyGoogle Scholar
  49. Rochebrune, A.-T., Mabille, J. (1889). Mollusques. Mission Scientifique du Cap Horn 1882–1883 (6):1–143. (Cited after Rodhouse and Yeatman 1990)Google Scholar
  50. Rodhouse, P. G. (1988). Squid fisheries in the South Atlantic. NERC News 5:20–21 (Natural Environment Research Council, Swindon, England)Google Scholar
  51. Rodhouse, P. G. (1989). Antarctic cephalopods — a living marine resource? Ambio 18:56–59Google Scholar
  52. Rodhouse, P. G. (1990). Cephalopod fauna of the Scotia Sea at South Georgia: potential for commercial exploitation and possible consequences. In: Kerry, K. R., Hempel, G. (eds.) Antarctic ecosystems. Ecological change and conservation. Springer-Verlag, Berlin, p. 289–298Google Scholar
  53. Rodhouse, P. G. (1991). Population structure of Martialia hyadesi (Cephalopoda: Ommastrephidae) at the Antarctic Polar Front and the Patagonian Shelf, South Atlantic. Bull. mar. Sci. 49: 404–418Google Scholar
  54. Rodhouse, P. G., Arnbom, T. R., Fedak, M. A., Yeatman, J., Murray, A. W. A. (1992). Cephalopod prey of the southern elephant seal Mirounga leonina L. Can. J. Zool. 70:1007–1015Google Scholar
  55. Rodhouse, P. G., Prince, P. A., Clarke, M. R., Murray, A. W. A. (1990). Cephalopod prey of the grey-headed albatross Diomedea chrysostoma. Mar. Biol. 104:353–362Google Scholar
  56. Rodhouse, P. G., Yeatman, J. (1990). Redescription of Martialia hyadesi Rochebrune and Mabille, 1889 (Mollusca: Cephalopoda) from the Southern ocean. Bull. Br. Mus. nat. Hist. (Zool.) 56:135–143Google Scholar
  57. Roeleveld, M. A. (1988). Generic interrelationships within the Ommastrephidae (Cephalopoda). In: Clarke, M. R., Trueman, E. R. (eds.). The Mollusca. Vol. 12. Paleontology and neontology of cephalopods. Academic Press, San Diego, p. 277–292Google Scholar
  58. Romero, M. C. L., Amaratunga, T. (1981). Preliminary results of a biochemical genetic population structure study of the squid Illex illecebrosus. NW. Atlant. Fish. Orgn (NAFO) scient. Counc. Res. Docums 81/1 x /103:1–42Google Scholar
  59. Roper, C. F. E., Sweeney, M. J., Naun, C. E. (1984). FAO species catalogue. Vol. 3. Cephalopods of the world. An annotated and illustrated guide to species of interest to fisheries. F.A.O. Fish. Synopsis 125(3):1–277Google Scholar
  60. Ryman, N., Utter, F. M. (eds.) (1987). Population genetics and fishery management. University of Washington Press, SeattleGoogle Scholar
  61. SAS Institute Inc. (1988). SAS/STAT users' guide. Release 6.03 edn. SAS Institute Inc., Cary, North CarolinaGoogle Scholar
  62. Schaal, B. A., Anderson, W. W. (1974). An outline of techniques for starch gel electrophoresis of enzymes from the American oyster Crassostrea virginica. Tech. Rep. Ser. Ga Sci. Cent. Savannah 74:3–19Google Scholar
  63. Selander, R. K. (1976). Genetic variation in natural populations. In: Ayala, F. J. (ed.) Molecular evolution. Sinauer Associates, Sunderland, Massachusetts, p. 21–45Google Scholar
  64. Selander, R. K., Kaufman, D. W. (1973). Self fertilisation and genetic population structure in a colonising land snail. Proc. natn. Acad. Sci. U.S.A. 70:1875–1877Google Scholar
  65. Shaw, C. R., Prasad, R. (1970). Starch gel electrophoresis of enzymes, a compilation of recipes. Biochem. Genet 4:297–320Google Scholar
  66. Smith, A. C. (1969). An electrophoretic study of the protein extracted in distilled water and saline from the eye lens nucleus of the squid Nototodarus haweiiensis (Berry). Comp. Biochem. Physiol. 30:551–559Google Scholar
  67. Smith, P. J. (1986). Low genetic variation in sharks (Chondrichthyes). Copeia 1986:202–206Google Scholar
  68. Smith, P. J., Mattlin, R. H., Roeleveld, M. A., Okutani, T. (1987). Arrow squids of the genus Nototodarus in New Zealand waters: systematics, biology and fisheries. N. Z. Jl mar. Freshwat. Res. 21:315–326Google Scholar
  69. Smith, P. J., Roberts, P. E., Hurst, R. J. (1981). Evidence for two species of arrow squid in the New Zealand fishery. N. Z. Jl mar. Freshwat. Res. 15:247–253Google Scholar
  70. Sneath, P. H. A., Sokal, R. R. (1973). Numerical taxonomy — the principles and practice of numerical classification. W. H. Freeman & Co., San FranciscoGoogle Scholar
  71. Summers, W. C. (1983). Loligo pealei. In: Boyle, P. R. (ed.). Cephalopod life cycles. Vol. 1. Academic Press, London, p. 162–178Google Scholar
  72. Suzuki, H., Ichikawa, M., Matsumoto, G. (1993). Indispensibility of squid for biological studies I. Genetic approach for elucidation of squid family. In: Okutani, T. (ed.) Recent advances in cephalopod fishery biology. Tokai University Press, Shimizu, Japan (in press)Google Scholar
  73. Swofford, D. L., Selander, R. B. (1981). BIOSYS-1: A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J. Hered. 72:281–283Google Scholar
  74. Thorpe, J. P. (1979). Enzyme variation and taxonomy: the estimation of sampling errors in measurement of interspecific genetic similarity. Biol. J. Linn. Soc. 11:369–386Google Scholar
  75. Thorpe, J. P. (1982). The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. A. Rev. Ecol. Syst. 13:139–168Google Scholar
  76. Thorpe, J. P. (1983). Enzyme variation, genetic distance, and evolutionary divergence in relation to levels of taxonomic separation. In: Oxford, G. S., Rollinson, D. (eds.) Protein polymorphism: adaptive and taxanomic significance. Academic Press, London, p. 131–152Google Scholar
  77. Thorpe, J. P., Havenhand, J. N., Patterson, K. (1986). Report of the University of Liverpool (Department of Marine Biology) to the Falkland Islands Development Corporation. Stock and species identities of Patagonian Shelf Illex. Falkland Islands Development Corporation, Port Stanley, Falkland IslandsGoogle Scholar
  78. Todd, C. D., Thorpe, J. P., Hadfield, M. G. (1991). Genetic structure of populations of the aplysiid opisthobranch Stylocheilus longicaudus (Quoy & Gaimard) around the shores of O'Ahu, Hawaii, J. mollusc. Stud. 57:153–166Google Scholar
  79. Uozumi, Y., Forch, E. C., Okazaki, T. (1991). Distribution and morphological characters of immature Martialia hyadesi (Cephalopoda: Oegopsida) in New Zealand waters. N. Z. Jl mar. Freshwat. Res. 25:275–282Google Scholar
  80. Voss, G. L. (1977). Present status and new trends in cephalopod systematics. Symp. zool. Soc. Lond. 38:49–60Google Scholar
  81. Ward, R. D., Beardmore, J. A. (1977). Protein variation in the plaice Pleuronectes platessa. Genet. Res. 30:45–62Google Scholar
  82. Woodruff, D. S., Mulvey, M., Saunders, W. B., Carpenter, M. P. (1983). Genetic variation in the cephalopod Nautilus belauensis. Proc. Acad. nat. Sci. Philad. 135:147–153Google Scholar
  83. Wormuth, J. H. (1976). The biogeography and numerical taxonomy of the oegopsid squid family Ommastrephidae in the Pacific Ocean. Bull. Scripps Instn Oceanogr. tech. Ser. 23:1–90Google Scholar
  84. Yeatman, J., Benzie, J. A. H. (1993). Cryptic speciation in Loligo from Northern Australia. In: Okutani, T. (ed.) Recent advances in cephalopod fishery biology. Tokai University Press, Shimizu, Japan (in press)Google Scholar
  85. Zouros, E. (1987). On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine molluscs. In: Rattazzi, M. C., Scandalios, J. G., Whitt, G. S. (eds.) Isozymes: current topics in biological and medical research. Vol. 15. Alan R. Liss Inc., New York, p. 225–270Google Scholar
  86. Zouros, E., Foltz, D. W. (1987). The use of allelic isozyme variation for the study of heterosis. In: Rattazzi, M. C., Scandalios, J. G., Whitt, G. S. (eds.) Isozymes: current topics in biological and medical research. Vol. 13. Alan R. Liss Inc., New York, p. 1–59Google Scholar
  87. Zuev, G. V., Nesis, K. N., Nigmatullin, Ch. M. (1975). Systematics and evolution of the genera Ommastrephes and Symplectoteuthes. Zool. Zh. 54:1468–1479Google Scholar
  88. Zuev, G. V., Nesis, K. N., Nigmatullin, Ch. M. (1976). Distribution of the genera Ommastrephes d'Orbigny, 1835, Sthenoteuthis Verril, 1880 and Todarodes Steenstrup, 1880 in the Atlantic Ocean. Byull. mosk. Obshch. Ispyt. Prir. (Sect. Biol.) 81:53–63Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • A. S. Brierley
    • 1
  • P. G. Rodhouse
    • 1
    • 2
  • J. P. Thorpe
    • 1
  • M. R. Clarke
    • 1
  1. 1.Department of Environmental and Evolutionary BiologyUniversity of Liverpool, Port Erin Marine LaboratoryPort ErinIsle of Man, British Isles
  2. 2.Marine Life Sciences DivisionBritish Antarctic SurveyCambridgeEngland

Personalised recommendations