Advertisement

Marine Biology

, Volume 143, Issue 5, pp 947–962 | Cite as

Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure

  • K. S. Kassahn
  • S. C. DonnellanEmail author
  • A. J. Fowler
  • K. C. Hall
  • M. Adams
  • P. W. Shaw
Article

Abstract

The giant Australian cuttlefish Sepia apama Gray, 1849 annually forms a massive and unique spawning aggregation in northern Spencer Gulf, South Australia, which has attracted commercial fishing interests in recent years. However, many basic life-history characteristics of S. apama are unknown, and anecdotal evidence suggests that there is more than one species. The present study assessed the population structure and species status of S. apama using data from allozyme electrophoresis, microsatellite loci, nucleotide sequences of the mitochondrial COXIII gene, multivariate morphometrics and colour patterns. Analyses of allozyme and microsatellite allele frequencies revealed two very divergent but geographically separated populations consisting of specimens from the east coast and southern Australia. However, the presence of a heterozygote in a putative contact zone between the east coast and southern Australia suggested that these populations were not reproductively isolated. Mitochondrial haplotypes seem to have introgressed further north into the contact zone than have nuclear alleles. Differences in colour patterns that previously had been attributed anecdotally to different geographic populations were, in fact, correlated with sexual dimorphism. These data are most consistent with S. apama being one species the populations of which were geographically isolated in the past (historical vicariance) and have come into secondary contact. Comparison of microsatellite allele frequencies among four South Australian samples indicated significant deviations from panmixia. South Australian samples were also reliably diagnosed by means of multivariate morphometrics. Significant differences in mantle length were observed among populations.

Keywords

Discriminant Function Analysis Mismatch Distribution Discriminant Function Analysis South Australia Mantle Length 
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.

Notes

Acknowledgements

This research was funded by the FRDC project number 98/151. We thank L. Triantafillos, R. Clementson, J. Brace, K. Rowling, H. Malcolm, J. North, J. Haddy, N. Kirby and E. Sporer for their assistance with the collection of samples, and K. Saint and T. Bertozzi for support with laboratory work. The experiments conducted in this project comply with Australian law.

References

  1. Avise JC (1996) Towards a regional conservation genetics perspective: phylogeography of faunas in the southeastern United States. In: Avise JC, Hamrick JL (eds) Conservation genetics: case histories from nature. Chapman and Hall, New York, pp 431–470Google Scholar
  2. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  3. Bailey KM (1997) Structural dynamics and ecology of flatfish populations. J Sea Res 37:269–280CrossRefGoogle Scholar
  4. Ballard JWO, Chernoff B, James AC (2002) Divergence of mitochondrial DNA is not corroborated by nuclear DNA, morphology, or behavior in Drosophila simulans. Evolution 56:527–545PubMedGoogle Scholar
  5. Barton NH (1979) Gene flow past a cline. Heredity 43:333–339Google Scholar
  6. Barton NH, Jones JS (1983) Mitochondrial DNA: new clues about evolution. Nature 306:317–318PubMedGoogle Scholar
  7. Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res (Amst) 43:35–44Google Scholar
  8. Belbin L (1994) PATN: pattern analysis package. Reference manual, C.S.I.R.O. Division of Wildlife and Ecology, Gungahlin, CanberraGoogle Scholar
  9. Bonnaud L, Boucherrodoni R, Monnerot M (1997) Phylogeny of cephalopods inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 7:44–54CrossRefPubMedGoogle Scholar
  10. Boucaud-Camou E, Boismery J (1991) The migrations of the cuttlefish (Sepia officinalis L) in the English Channel. Centre de Publications de l'Université de Caen, Caen, pp 179–189Google Scholar
  11. Brierley AS, Thorpe JP, Pierce GJ, Clarke MR, Boyle PR (1995) Genetic variation in the neritic squid Loligo forbesi (Myopsida, Loliginidae) in the Northeast Atlantic Ocean. Mar Biol 122:79–86Google Scholar
  12. Caddy JF, Rodhouse PG (1998) Cephalopod and groundfish landings: evidence for ecological change in global fisheries? Rev Fish Biol Fish 8:431–444Google Scholar
  13. Cappo M, Walters CJ, Lenanton RC (2000) Estimation of rates of migration, exploitation and survival using tag recovery data for Western Australian "salmon" (Arripis truttaceus: Arripidae: Percoidei). Fish Res (Amst) 44:207–217Google Scholar
  14. Carvalho GR, Hauser L (1994) Molecular genetics and the stock concept in fisheries. Rev Fish Biol Fish 4:326–350Google Scholar
  15. Carvalho GR, Loney KH (1989) Biochemical genetic studies on the Patagonian squid Loligo gahi d'Orbigny. I. Electrophoretic survey of genetic variability. J Exp Mar Biol Ecol 126:231–241Google Scholar
  16. Carvalho GR, Pitcher TJ (1989) Biochemical genetic studies on the Patagonian squid Loligo gahi d'Orbigny. II. Population structure in Falkland waters using isozymes, morphometrics and life history data. J Exp Mar Biol Ecol 126:243–258Google Scholar
  17. Carvalho GR, Thompson A, Stoner AL (1992) Genetic diversity and population differentiation of the shortfin squid Illex argentinus in the south-west Atlantic. J Exp Mar Biol Ecol 158:105–121Google Scholar
  18. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedGoogle Scholar
  19. Colgan DJ, Paxton JR (1997) Biochemical genetics and recognition of a western stock of the common gemfish, Rexea solandri (Scombroidea, Gempylidae), in Australia. Mar Freshw Res 48:103–118Google Scholar
  20. Constanza MC, Afifi AA (1979) Comparison of stopping rules in forward stepwise discriminant analysis. J Am Stat Assoc 74:777–785Google Scholar
  21. Dartnall AJ (1974) Littoral biogeography. In: Williams WD (ed) Biogeography and ecology in Tasmania. Junk, The Hague, pp 171–194Google Scholar
  22. Donnellan SC, Aplin KP (1989) Resolution of cryptic species in the New Guinean lizard, Sphenomorphus jobiensis (Scincidae) by electrophoresis. Copeia 1989:81–88Google Scholar
  23. Ferris SD, Sage RD, Huan CM, Nielson JT, Ritte U, Wilson AC (1983) Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci USA 80:2290–2294PubMedGoogle Scholar
  24. Forsythe JW, Derusha RH, Hanlon RT (1994) Growth, reproduction and life span of Sepia officinalis (Cephalopoda, Mollusca) cultured through seven consecutive generations. J Zool 233:175–192Google Scholar
  25. Forsythe JW, Walsh LS, Turk PE, Lee PG (2001) Impact of temperature on juvenile growth and age at first egg-laying of the Pacific reef squid Sepioteuthis lessoniana reared in captivity. Mar Biol 138:103–112CrossRefGoogle Scholar
  26. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  27. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
  28. Goodman SJ (1997) RST CALC—a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol Ecol 6:881–885Google Scholar
  29. Goudet J, Raymond M, Demeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  30. Hall KC (2002) Cuttlefish (Sepia apama). Fishery Assessment Report to PIRSA for the Marine Scalefish Fishery Management Committee, University of Adelaide and SARDI Aquatic Sciences, AdelaideGoogle Scholar
  31. Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545CrossRefGoogle Scholar
  32. Hamabe M, Shimizu T (1966) Ecological studies on the common squid Todarodes pacificus Steenstrup mainly in southwestern waters of the Sea of Japan. Bull Jpn Sea Reg Fish Res Lab 16:13–55Google Scholar
  33. Hare MP, Avise JC (1996) Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305–2315Google Scholar
  34. Hare MP, Avise JC (1998) Population structure in the American oyster as inferred by nuclear gene genealogies. Mol Biol Evol 15:119–128PubMedGoogle Scholar
  35. Hare MP, Karl SA, Avise JC (1996) Anonymous nuclear DNA markers in the American oyster and their implications for the heterozygote deficiency phenomenon in marine bivalves. Mol Biol Evol 13:334–345PubMedGoogle Scholar
  36. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  37. Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxf Surv Evol Biol 7:69–128Google Scholar
  38. Harrison RG, Rand DM, Wheeler WC (1987) Mitochondrial DNA variation in field crickets across a narrow hybrid zone. Mol Biol Evol 4:144–158Google Scholar
  39. Joseph L, Wilke T, Alpers D (2002) Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield's bronze-cuckoo Chalcites basalis of Australia. Mol Ecol 11:829–837CrossRefPubMedGoogle Scholar
  40. King M (1995) Fisheries biology, assessment and management. Blackwell, VictoriaGoogle Scholar
  41. Kristensen TK (1982) Multivariate statistical analysis of geographic variation in the squid Gonatus fabricii Lichtenstein, 1818 (Mollusca: Cephalopoda). Malacologia 22:581–586Google Scholar
  42. Leslie RW, Grant WS (1990) Lack of congruence between genetic and morphological stock structure of the southern African anglerfish Lophius vomerinus. S Afr J Mar Sci 9:379–398Google Scholar
  43. Lunneborg CE (1994) Modeling experimental and observational data. Duxbury, Belmont, Calif.Google Scholar
  44. Mantel N (1967) The detection of disease clustering and a generalised regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  45. Martínez P, Sanjuan A, Guerra A (2002) Identification of Illex coindetii, I. illecebrosus and I. argentinus (Cephalopoda: Ommastrephidae) throughout the Atlantic Ocean; by body and beak characters. Mar Biol 141:131–143CrossRefGoogle Scholar
  46. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215PubMedGoogle Scholar
  47. Moran C (1979) The structure of the hybrid zone in Caledia captiva. Heredity 42:13–32Google Scholar
  48. Moran C, Wilkinson P, Shaw DD (1980) Allozyme variation across a narrow hybrid zone in the grasshopper, Caledia captiva. Heredity 44:69–81Google Scholar
  49. Moritz C (1994) Applications of mitochondrial DNA analysis in conservation—a critical review. Mol Ecol 3:401–411Google Scholar
  50. Murata M (1989) Population assessment, management and fishery forecasting for the Japanese common squid, Todarodes pacificus. In: Caddy JF (ed) Marine invertebrate fisheries: their assessment and management. Wiley, New York, pp 613–636Google Scholar
  51. Murphy RW, Sites JW, Buth DG, Haufler CH (1996) Proteins: isozyme electrophoresis. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer, Sunderland, Mass., pp 51–120Google Scholar
  52. Palumbi SR (1996) What can molecular genetics contribute to marine biogeography—an urchins tale. J Exp Mar Biol Ecol 203:75–92Google Scholar
  53. Pérez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cepahlopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424CrossRefPubMedGoogle Scholar
  54. Petry D (1983) The effect on neutral gene flow of selection at a linked locus. Theor Popul Biol 23:300–313PubMedGoogle Scholar
  55. Piatkowski U, Pierce GJ, Morais da Cunha M (2001) Impact of cephalopods in the food chain and their interaction with the environment and fisheries: an overview. Fish Res (Amst) 52:5–10Google Scholar
  56. Pierce GJ, Guerra A (1994) Stock assessment methods used for cephalopod fisheries. Fish Res (Amst) 21:255–285Google Scholar
  57. Pierce GJ, Thorpe RS, Hastie LC, Brierley AS, Guerra A, Boyle PR, Jamieson R, Avila P (1994) Geographic variation in Loligo forbesi in the Northeast Atlantic Ocean—Analysis of morphometric data and tests of causal hypotheses. Mar Biol 119:541–547Google Scholar
  58. Poore GCB (1994) Marine biogeography of Australia. In: Hammond LS, Synnot RN (eds) Marine biology. Longman Cheshire, Melbourne, pp 189–212Google Scholar
  59. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  60. Rambaut A (1996) Se-Al: sequence alignment editor, version 1.0, alpha 1. University of Oxford, OxfordGoogle Scholar
  61. Raymond M, Rousset F (1995a) GENEPOP, version 1.2—populations genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  62. Raymond M, Rousset F (1995b) An exact test for population differentiation. Evolution 49:1280–1283Google Scholar
  63. Reid AL (2000) Australian cuttlefishes (Cephalopoda: Sepiidae): the 'doratosepion' species complex. Invertebr Taxon 14:1–76CrossRefGoogle Scholar
  64. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225Google Scholar
  65. Richardson BJ, Baverstock PR, Adams M (1986) Allozyme electrophoresis: a handbook for animal systematics and population studies. Academic, SydneyGoogle Scholar
  66. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615Google Scholar
  67. Rogers JS (1972) Measures of genetic similarity and genetic distance. Stud Genet 7213:145–153Google Scholar
  68. Rozas J, Rozas R (1999) DnaSP, version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175CrossRefPubMedGoogle Scholar
  69. Shaw PW (2003) Polymorphic microsatellite DNA markers for the assessment of genetic diversity and paternity testing in the giant cuttlefish, Sepia apama (Cephalopoda). Conserv Genet (in press)Google Scholar
  70. 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 8:407–417Google Scholar
  71. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  72. Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, Mass.Google Scholar
  73. Tabachnik BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, BostonGoogle Scholar
  74. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  75. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  76. Tompsett DH (1939) Sepia. Williams and Norgate, LondonGoogle Scholar
  77. Triantafillos L, Adams M (2001) Allozyme analysis reveals a complex population structure in the southern calamary Sepioteuthis australis from Australia and New Zealand. Mar Ecol Prog Ser 212:193–209Google Scholar
  78. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  79. Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26Google Scholar
  80. Yeatman J, Benzie JAH (1994) Genetic structure and distribution of Photololigo spp. in Australia. Mar Biol 118:79–87Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • K. S. Kassahn
    • 1
  • S. C. Donnellan
    • 2
    Email author
  • A. J. Fowler
    • 3
  • K. C. Hall
    • 3
    • 5
  • M. Adams
    • 2
  • P. W. Shaw
    • 4
  1. 1.Department of Environmental BiologyUniversity of AdelaideAdelaideAustralia
  2. 2.Evolutionary Biology UnitSouth Australian MuseumAdelaideAustralia
  3. 3.SARDI Aquatic SciencesWest BeachAustralia
  4. 4.Environmental and Evolutionary Biology Research Group, School of Biological SciencesUniversity of LondonEghamUK
  5. 5.Department of Environmental BiologyUniversity of AdelaideAdelaideAustralia

Personalised recommendations