Skip to main content
Log in

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

  • Published:
Marine Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • 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. 1–18

    Google Scholar 

  • 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. 169:113–121

    Google Scholar 

  • Amaratunga, T. (1987). Population biology. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol. 2. Comparative reviews. Academic Press, London, p. 239–252

    Google Scholar 

  • Anonymous. (1989). Falkland Islands interim conservation and management zone. Fisheries report '87/88. Falkland Islands Government, Port Stanley, Falkland Islands

  • Arnold, C. P. (1979). Squid, a review of their biology and fisheries. Lab. Leafl. Minist. Agric. Fish. Fd Direct. Fish. Res., Lowestoft 48:1–37

    Google Scholar 

  • 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 29:215–233

    Google Scholar 

  • Avise, J. C. (1974). Systematic value of electrophoretic data. Syst. Zool. 23: 465–481

    Google Scholar 

  • 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. 3–26

    Google Scholar 

  • Bonnell, M. L., Selander, R. K. (1974). Elephant seals, genetic variation and near extinction. Science, N.Y. 184:908–909

    Google Scholar 

  • Boyer, S. H., Fainer, D. C., Naughton, M. A. (1963). Myoglobin: inherited structural variation in man. Science, N.Y. 140:1228–1231

    Google Scholar 

  • Brewer, G. J. (1970). An introduction to isozyme technique. Academic Press, New York

    Google Scholar 

  • Brierley, A. S. (1992). Aspects of genetic diversity and population structure in squid. Unpublished thesis. University of Liverpool, Port Erin, Isle of Man

    Google Scholar 

  • 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 

  • 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. 126:231–241

    Google Scholar 

  • 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. 126:243–258

    Google Scholar 

  • 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. 158:105–121

    Google Scholar 

  • Chakraborty, R., Fuerst, P. A., Nei, M. (1978). Statistical studies on protein polymorphism in natural populations II. Gene differentiation between populations. Genetics Austin, Tex. 88:367–390

    Google Scholar 

  • 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. 169:123–133

    Google Scholar 

  • Clarke, M. R. (1966). A review of the systematics and ecology of oecanic squids. Adv. mar. Biol. 4: 91–300

    Google Scholar 

  • Csirke, J. (1987). The Patagonian fishery resources and the offshore fisheries in the South-West Atlantic. F.A.O. Fish. tech. Pap. 286: 1–75

    Google Scholar 

  • 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. 2:249–257

    Google Scholar 

  • Everhart, W. H., Eipper, A. W., Young, W. D. (1975). Principles of fishery science. Cornell University Press, Ithaca, N.Y.

    Google Scholar 

  • Fildes, R. A., Harris, H. (1966). Genetically determined variation of adenylate kinase in man. Nature, London. 209: 261–263

    Google Scholar 

  • 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 177:287–294

    Google Scholar 

  • Harris, H., Hopkinson, D. A. (1977). Handbook of enzyme electrophoresis in human genetics. North Holland Publishing Co., Amsterdam

    Google Scholar 

  • Hartl, D. L., Clark, A. G. (1989). Principles of population genetics. 2nd ed. Sinauer Associates, Sunderland, Mass.

    Google Scholar 

  • 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 38:1838–1855

    Google Scholar 

  • 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. 46:145–152

    Google Scholar 

  • 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, Louisiana

    Google Scholar 

  • Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press, London

    Google Scholar 

  • Koehn, R. K., Hilbish, T. J. (1987). The adaptive importance of genetic variation. Am. Scient. 75:134–141

    Google Scholar 

  • 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:275–277

    Google Scholar 

  • 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) 79/11/38:1–40

    Google Scholar 

  • Mallet, A. L., Haley, L. E. (1983). Effects of inbreeding on larval and spat performance in the American oyster. Aquaculture, Amsterdam 33:229–235

    Google Scholar 

  • Maynard Smith, J. (1989). Evolutionary genetics. Oxford University Press, Oxford

    Google Scholar 

  • 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 

  • Nei, M. (1972). Genetic distance between populations. Am. Nat. 106:283–292

    Google Scholar 

  • Nei, M. (1987). Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nesis, K. N. (1987). Cephalopods of the world. T.F.H. Publications Inc., Neptune, City, N.J.

    Google Scholar 

  • Nevo, E. (1978). Genetic variation in natural populations: patterns and theory. Theor. Popul. Biol. 13:121–177

    Google Scholar 

  • 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. 239–282

    Google Scholar 

  • 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. 13–213

    Google Scholar 

  • 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. 84:508–511

    Google Scholar 

  • Patterson, K. (1987). Fishy events in the Falklands. New Scient. 1562:44–48

    Google Scholar 

  • Poulik, M. D. (1957). Starch gel electrophoresis in a discontinuous system of buffers. Nature, Lond. 180:1477–1479

    Google Scholar 

  • 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. 253–275

    Google Scholar 

  • 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 

  • Richardson, B. J., Baverstock, P. R., Adams, M. (1986). Allozyme electrophoresis — a handbook for animal systematics and population studies. Academic Press, Sydney

    Google Scholar 

  • 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 

  • Rodhouse, P. G. (1988). Squid fisheries in the South Atlantic. NERC News 5:20–21 (Natural Environment Research Council, Swindon, England)

    Google Scholar 

  • Rodhouse, P. G. (1989). Antarctic cephalopods — a living marine resource? Ambio 18:56–59

    Google Scholar 

  • 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. 289–298

    Google Scholar 

  • 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: 404–418

    Google Scholar 

  • 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. 70:1007–1015

    Google Scholar 

  • 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. 104:353–362

    Google Scholar 

  • 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.) 56:135–143

    Google Scholar 

  • 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. 277–292

    Google Scholar 

  • 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 /103:1–42

    Google Scholar 

  • 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):1–277

    Google Scholar 

  • Ryman, N., Utter, F. M. (eds.) (1987). Population genetics and fishery management. University of Washington Press, Seattle

    Google Scholar 

  • SAS Institute Inc. (1988). SAS/STAT users' guide. Release 6.03 edn. SAS Institute Inc., Cary, North Carolina

    Google Scholar 

  • 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 74:3–19

    Google Scholar 

  • Selander, R. K. (1976). Genetic variation in natural populations. In: Ayala, F. J. (ed.) Molecular evolution. Sinauer Associates, Sunderland, Massachusetts, p. 21–45

    Google Scholar 

  • 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. 70:1875–1877

    Google Scholar 

  • Shaw, C. R., Prasad, R. (1970). Starch gel electrophoresis of enzymes, a compilation of recipes. Biochem. Genet 4:297–320

    Google Scholar 

  • 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. 30:551–559

    Google Scholar 

  • Smith, P. J. (1986). Low genetic variation in sharks (Chondrichthyes). Copeia 1986:202–206

    Google Scholar 

  • 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. 21:315–326

    Google Scholar 

  • 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. 15:247–253

    Google Scholar 

  • Sneath, P. H. A., Sokal, R. R. (1973). Numerical taxonomy — the principles and practice of numerical classification. W. H. Freeman & Co., San Francisco

    Google Scholar 

  • Summers, W. C. (1983). Loligo pealei. In: Boyle, P. R. (ed.). Cephalopod life cycles. Vol. 1. Academic Press, London, p. 162–178

    Google Scholar 

  • 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 

  • 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. 72:281–283

    Google Scholar 

  • Thorpe, J. P. (1979). Enzyme variation and taxonomy: the estimation of sampling errors in measurement of interspecific genetic similarity. Biol. J. Linn. Soc. 11:369–386

    Google Scholar 

  • Thorpe, J. P. (1982). The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. A. Rev. Ecol. Syst. 13:139–168

    Google Scholar 

  • 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. 131–152

    Google Scholar 

  • 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 Islands

    Google Scholar 

  • 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. 57:153–166

    Google Scholar 

  • 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. 25:275–282

    Google Scholar 

  • Voss, G. L. (1977). Present status and new trends in cephalopod systematics. Symp. zool. Soc. Lond. 38:49–60

    Google Scholar 

  • Ward, R. D., Beardmore, J. A. (1977). Protein variation in the plaice Pleuronectes platessa. Genet. Res. 30:45–62

    Google Scholar 

  • Woodruff, D. S., Mulvey, M., Saunders, W. B., Carpenter, M. P. (1983). Genetic variation in the cephalopod Nautilus belauensis. Proc. Acad. nat. Sci. Philad. 135:147–153

    Google Scholar 

  • 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. 23:1–90

    Google Scholar 

  • 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 

  • 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. 225–270

    Google Scholar 

  • 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. 1–59

    Google Scholar 

  • Zuev, G. V., Nesis, K. N., Nigmatullin, Ch. M. (1975). Systematics and evolution of the genera Ommastrephes and Symplectoteuthes. Zool. Zh. 54:1468–1479

    Google Scholar 

  • 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.) 81:53–63

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. Mauchline, Oban

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brierley, A.S., Rodhouse, P.G., Thorpe, J.P. et al. Genetic evidence of population heterogeneity and cryptic speciation in the ommastrephid squid Martialia hyadesi from the Patagonian Shelf and Antarctic Polar Frontal Zone. Marine Biology 116, 593–602 (1993). https://doi.org/10.1007/BF00355478

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00355478

Keywords

Navigation