Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Patterns of connectivity and population structure of the southern calamary Sepioteuthis australis in southern Australia

Timothy M. Smith A C , Corey P. Green B and Craig D. H. Sherman A
+ Author Affiliations
- Author Affiliations

A Centre for Integrated Ecology, School of Life and Environmental Sciences, Deakin University, 96 Pigdon Road, Waurn Ponds, Vic 3216, Australia.

B Department of Environment and Primary Industries, 2a Bellarine Highway, Queenscliff, Vic 3225, Australia.

C Corresponding author. Email: tim.smith@deakin.edu.au

Marine and Freshwater Research 66(10) 942-947 https://doi.org/10.1071/MF14328
Submitted: 11 July 2014  Accepted: 4 December 2014   Published: 19 March 2015

Abstract

The southern calamary, Sepioteuthis australis, is a commercially and recreationally important inshore cephalopod endemic to southern Australia and New Zealand. Typical of other cephalopods, S. australis has a short life span, form nearshore spawning aggregations and undergo direct development. Such life history traits may restrict connectivity between spawning grounds creating highly structured and genetically differentiated populations that are susceptible to population crashes. Here we use seven polymorphic microsatellite markers to assess connectivity and population structure of S. australis across a large part of its geographic range in Australia. Little genetic differentiation was found between sampling locations. Overall, FST was low (0.005, 95% CI = <0.001–0.011) and we detected no significant genetic differentiation between any of the locations sampled. There was no strong relationship between genetic and geographical distance, and our neighbour joining analysis did not show clustering of clades based on geographical locations. Similarly, network analysis showed strong connectivity amongst most locations, in particular, Tasmania appears to be well connected with several other locations and may act as an important source population. High levels of gene flow and connectivity between S. australis sampling sites across Australia are important for this short-lived species, ensuring resilience against spatial and temporal mortality fluctuations.

Additional keywords: invertebrate, microsatellites, null alleles, population resilience, squid.


References

Andre, J., Lyle, J., and Hartman, K. (2014) Tasmanian scalefish fishery assessment 2010/2012. IMAS, Hobart.

Astanei, I., Gosling, E., Wilson, J., and Powell, E. (2005). Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas). Molecular Ecology 14, 1655–1666.
Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVeqsbc%3D&md5=2aca8406136438d3cc09a09834391d00CAS | 15836640PubMed |

Basson, M., and Beddington, J. R. (1993). Risks and uncertainties in the management of a single-cohort squid fishery: the Falkland Islands Illex fishery as an example. Canadian Special Publication of Fisheries and Aquatic Sciences 120, 253–259.

Boyle, P., and Rodhouse, P. G. (2005) ‘Cephalopods – Ecology and Fisheries.’ (Blackwell Science: Oxford, UK.)

Buresch, K. C., Gerlach, G., and Hanlon, R. T. (2006). Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter. Marine Ecology Progress Series 310, 263–270.
Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFSrsbY%3D&md5=16f529cf6d5ec5a6d583883c3d744cfeCAS |

Chapuis, M. P., and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621–631.
Microsatellite null alleles and estimation of population differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtleku7c%3D&md5=26e281717e3ceddbac87bdb2cd9bfb71CAS | 17150975PubMed |

Dempster, A. P., Laird, N. M., and Rubin, D. B. (1977). Maximum likelihood from incomplete data via EM algorithm. Journal of the Royal Statistical Society – B. Methodological 39, 1–38.

Department of Primary Industries (2009) Fisheries Victoria commercial fish production information bulletin 2009. Fisheries Victoria, Queenscliff, Victoria, Australia.

Fogarty, M. J., Sissenwine, M. P., and Cohen, E. B. (1991). Recruitment variability and the dynamics of exploited marine populations. Trends in Ecology & Evolution 6, 241–246.
Recruitment variability and the dynamics of exploited marine populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7hsVemsQ%3D%3D&md5=b215f7667f01beee80abce781b73d762CAS |

Fowler, A. J., McGarvey, A., Steer, M. A., and Freenstra, J. E. (2013) The South Australian marine scalefish fishery status report – Analysis of fisheries statistics for 2012/2013. South Australian Research and Development Institute, Adelaide.

Freeland, J. R. (2005) ‘Molecular Ecology.’ pp. 112–115. (Wiley: Chichester, UK.)

Garoia, F., Guarniero, I., Ramsak, A., Ungaro, N., Landi, M., Piccinetti, C., Mannini, P., and Tinti, F. (2004). Microsatellite DNA variation reveals high gene flow and panmictic populations in the Adriatic shared stocks of the European squid and cuttlefish (Cephalopoda). Heredity 93, 166–174.
Microsatellite DNA variation reveals high gene flow and panmictic populations in the Adriatic shared stocks of the European squid and cuttlefish (Cephalopoda).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFCqsb8%3D&md5=f84d8b56985a245d5ffe1b8eeab28a58CAS | 15150540PubMed |

Gunderson, L. H. (2000). Ecological resilience – In theory and application. Annual Review of Ecology and Systematics 31, 425–439.
Ecological resilience – In theory and application.Crossref | GoogleScholarGoogle Scholar |

Ibáñez, C. M., Cubillos, L. A., Tafur, R., Argüelles, J., Yamashiro, C., and Poulin, E. (2011). Genetic diversity and demographic history of Dosidicus gigas (Cephalopoda: Ommastrephidae) in the Humboldt Current System. Marine Ecology Progress Series 431, 163–171.
Genetic diversity and demographic history of Dosidicus gigas (Cephalopoda: Ommastrephidae) in the Humboldt Current System.Crossref | GoogleScholarGoogle Scholar |

Ibáñez, C. M., Argüelles, J., Yamashiro, C., Adasme, L., Céspedes, R., and Poulin, E. (2012). Spatial genetic structure and demographic inference of the Patagonian squid Doryteuthis gahi in the south-eastern Pacific Ocean. Journal of the Marine Biological Association of the United Kingdom 92, 197–203.

Jensen, J. L., Bohonak, A. J., and Kelley, S. T. (2005). Isolation by distance, web service. BMC Genetics 6, 13.
Isolation by distance, web service.Crossref | GoogleScholarGoogle Scholar | 15760479PubMed |

Kang, J. H., Kim, Y. K., Park, J. Y., An, C. M., and Jun, J. C. (2012). Development of microsatellite markers to genetically differentiate populations of Octopus minor from Korea and China. Molecular Biology Reports 39, 8277–8286.
Development of microsatellite markers to genetically differentiate populations of Octopus minor from Korea and China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xpt12jtL4%3D&md5=3d3c993c3d4a3102221074c6ce2e2537CAS | 22707143PubMed |

Kivelä, M., Arnaud-Haond, S., and Saramäki, J. (2015). EDENetworks: a user-friendly software to build and analyse networks in biogeography, ecology and population genetics. Molecular Ecology Resources 15, 117–122.
EDENetworks: a user-friendly software to build and analyse networks in biogeography, ecology and population genetics.Crossref | GoogleScholarGoogle Scholar | 24902875PubMed |

Lemer, S., Rochel, E., and Planes, S. (2011). Correction method for null alleles in species with variable microsatellite flanking regions, a case study of the black-lipped pearl Oyster Pinctada margaritifera. The Journal of Heredity 102, 243–246.
Correction method for null alleles in species with variable microsatellite flanking regions, a case study of the black-lipped pearl Oyster Pinctada margaritifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlaksro%3D&md5=510b118aced45030131dd1fa77763a64CAS | 21220742PubMed |

Moltschaniwskyj, N. A., and Steer, M. A. (2004). Spatial and seasonal variation in reproductive characteristics and spawning of southern calamary (Sepioteuthis australis): spreading the mortality risk. ICES Journal of Marine Science 61, 921–927.
Spatial and seasonal variation in reproductive characteristics and spawning of southern calamary (Sepioteuthis australis): spreading the mortality risk.Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T., and Moltschaniwskyj, N. A. (2006). Life history of a short-lived squid (Sepioteuthis australis): resource allocation as a function of size, growth, maturation, and hatching season. ICES Journal of Marine Science 63, 995–1004.

Pecl, G. T., Tracey, S. R., Danyushevsky, L., Wotherspoon, S., and Moltschaniwskyj, N. A. (2011). Elemental fingerprints of southern calamary (Sepioteuthis australis) reveal local recruitment sources and allow assessment of the importance of closed areas. Canadian Journal of Fisheries and Aquatic Sciences 68, 1351–1360.
Elemental fingerprints of southern calamary (Sepioteuthis australis) reveal local recruitment sources and allow assessment of the importance of closed areas.Crossref | GoogleScholarGoogle Scholar |

Reichow, D., and Smith, M. J. (2001). Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens. Molecular Ecology 10, 1101–1109.
Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktFKitb8%3D&md5=ac1eae800ac7bd4a39ff617147bb2124CAS | 11380869PubMed |

Shaw, P. W., Pierce, G. J., and Boyle, P. R. (1999). Subtle population structuring within a highly vagil marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Molecular Ecology 8, 407–417.
Subtle population structuring within a highly vagil marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtVKht7s%3D&md5=6f3a6acea7b468d33d79c5868f2bf320CAS |

Shaw, P. W., Hendrickson, L., McKeown, N. J., Stonier, T., Naud, M. J., and Sauer, W. H. H. (2010). Discrete spawning aggregations of loliginid squid do not represent genetically distinct populations. Marine Ecology Progress Series 408, 117–127.
Discrete spawning aggregations of loliginid squid do not represent genetically distinct populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVelsr0%3D&md5=2877a32ba510d1df0ad7b6fc0fac1862CAS |

Steer, M. A., Lloyd, M. T., and Jackson, W. B. (2007). Assessing the feasibility of using ‘by-product’ data as a pre-recruit index in South Australia’s southern calamary (Sepioteuthis australis) fishery. Fisheries Research 88, 42–50.
Assessing the feasibility of using ‘by-product’ data as a pre-recruit index in South Australia’s southern calamary (Sepioteuthis australis) fishery.Crossref | GoogleScholarGoogle Scholar |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA:6 molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA:6 molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=e8c149c24c63ea752681aeac2f06680fCAS | 24132122PubMed |

Triantafillos, L., and Adams, M. (2001). Allozyme analysis reveals a complex population structure in the southern calamary Sepioteuthis australis from Australia and New Zealand. Marine Ecology Progress Series 212, 193–209.
Allozyme analysis reveals a complex population structure in the southern calamary Sepioteuthis australis from Australia and New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Gisb0%3D&md5=448d7abc04a374c509b74f3d73476fd5CAS |

Van Camp, L. M., Saint, K. M., Donnellan, S., Havenhand, J. N., and Fairweather, P. G. (2003). Polymorphic microsatellite markers for paternity assessment in southern calamari Sepioteuthis australis (Cephalopoda: Loliginidae). Molecular Ecology Notes 3, 654–655.
Polymorphic microsatellite markers for paternity assessment in southern calamari Sepioteuthis australis (Cephalopoda: Loliginidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks12rug%3D%3D&md5=b08233213eef013f0348a6b011da0fb6CAS |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
Micro-checker: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=9eba570f66de684e1491071ac94a19b1CAS |

Van Oppen, M. J. H., and Gates, R. D. (2006). Conservation genetics and the resilience of reef-building corals. Molecular Ecology 15, 3863–3883.
Conservation genetics and the resilience of reef-building corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSmsrvE&md5=7ab3b895392977e57c48267f27fe4c57CAS |

Winstanley, R. H. (1983). Australian celphalopod resources. Memoirs of Museum Victoria 44, 243–253.