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RESEARCH ARTICLE

Population structure in a wide-ranging coastal teleost (Argyrosomus japonicus, Sciaenidae) reflects marine biogeography across southern Australia

Thomas C. Barnes A G , Claudia Junge A , Steven A. Myers A , Mathew D. Taylor B C , Paul J. Rogers D , Greg J. Ferguson D , Jason A. Lieschke E , Stephen C. Donnellan F and Bronwyn M. Gillanders A
+ Author Affiliations
- Author Affiliations

A Southern Seas Ecology Laboratories, Darling Building, School of Biological Sciences and Environment Institute, University of Adelaide, SA 5005, Australia.

B School of Biological, Earth and Environmental Science, University of New South Wales, Sydney, NSW 2052, Australia.

C Port Stephens Fisheries Institute, New South Wales Department of Primary Industries, Taylors Beach, NSW 2316, Australia.

D South Australian Research and Development Institute (Aquatic Sciences), PO Box 120, Henley Beach, SA 5024, Australia.

E Arthur Rylah Institute for Environmental Research, Department of Environment, Land, Water and Planning, 123 Brown Street, Heidelberg, Vic. 3084, Australia.

F South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

G Corresponding author. Email: thomas.barnes@adelaide.edu.au

Marine and Freshwater Research 67(8) 1103-1113 https://doi.org/10.1071/MF15044
Submitted: 3 February 2015  Accepted: 6 June 2015   Published: 10 September 2015

Abstract

Population structure in marine teleosts is often investigated to aid conservation and fisheries management (e.g. to assess population structure to inform restocking programs). We assessed genetic population structure of the important estuary-associated marine fish, mulloway (Argyrosomus japonicus), within Australian waters and between Australia and South Africa. Genetic variation was investigated at 13 polymorphic microsatellite markers. FST values and Bayesian estimates in STRUCTURE suggested population differentiation of mulloway within Australia and confirm strong differentiation between South Africa and Australia. The 12 Australian sample sets fell into one of four spatially separated genetic clusters. Initially, a significant signal of isolation-by-distance (IBD) was evident among Australian populations. However, further investigation by decomposed-pairwise-regression (DPR) suggested five sample sets were influenced more by genetic-drift, rather than gene-flow and drift equilibrium, as expected in strong IBD cases. Cryptic oceanographic and topographical influences may isolate mulloway populations from south-western Australia. The results demonstrate that DPR is suitable to assess population structure of coastal marine species where barriers to gene flow may be less obvious than in freshwater systems. Information on the relative strengths of gene flow and genetic drift facilitates a more comprehensive understanding of the evolutionary forces that lead to population structure, which in turn informs fisheries and assists conservation management. Large-bodied predatory scale-fish may be under increasing pressure on a global scale, owing to a variety of anthropogenic reasons. In southern Australia, the iconic sciaenid A. japonicus (mulloway, jewfish or kob) is no exception. Despite the species supporting important fisheries, much of its ecology is poorly understood. It is possible that a greater understanding of their genetic population structure can help ensure a sustainable future for the only southern Australian sciaenid.

Additional keywords: jewfish, kob, population genetics.


References

Archangi, B. (2008) Levels and patterns of genetic diversity in wild and cultured populations of mulloway (Argyrosomus japonicus) using mitochondrial DNA and microsatellites. Ph.D. Thesis, Queensland University of Technology, Brisbane.

Barnes, T. C., and Gillanders, B. M. (2013). Combined effects of extrinsic and intrinsic factors on otolith chemistry: implications for environmental reconstructions. Canadian Journal of Fisheries and Aquatic Sciences 70, 1159–1166.
Combined effects of extrinsic and intrinsic factors on otolith chemistry: implications for environmental reconstructions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCisb3J&md5=25ec3c304cfa0ec3751b83ae5395b9baCAS |

Barnes, T. C., Izzo, C., Bertozzi, T., Saint, K. M., Donnellan, S., Hammer, M. P., and Gillanders, B. M. (2014). Development of 15 microsatellite loci from mulloway, Argyrosomus japonicus (Pisces: Sciaenidae) using next generation sequencing and an assessment of their cross amplification in other sciaenids. Conservation Genetics Resources 6, 345–348.
Development of 15 microsatellite loci from mulloway, Argyrosomus japonicus (Pisces: Sciaenidae) using next generation sequencing and an assessment of their cross amplification in other sciaenids.Crossref | GoogleScholarGoogle Scholar |

Battaglene, S. C., and Talbot, R. B. (1994). Hormone induction and larval rearing of mulloway, Argyrosomus hololepidotus (Pisces: Sciaenidae). Aquaculture 126, 73–81.
Hormone induction and larval rearing of mulloway, Argyrosomus hololepidotus (Pisces: Sciaenidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhvFSgtb4%3D&md5=26efcb2a69cbd0f73e9c2e5acdf767f2CAS |

Begg, G. A., and Waldman, J. R. (1999). An holistic approach to fish stock identification. Fisheries Research 43, 35–44.
An holistic approach to fish stock identification.Crossref | GoogleScholarGoogle Scholar |

Bilgmann, K., Möller, L. M., Harcourt, R. G., Gibbs, S. E., and Beheregaray, L. B. (2007). Genetic differentiation in bottlenose dolphins from South Australia: association with local oceanography and coastal geography. Marine Ecology Progress Series 341, 265–276.
Genetic differentiation in bottlenose dolphins from South Australia: association with local oceanography and coastal geography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXps1Sis70%3D&md5=c7f9f2706329e42fe95e91e9e8eaeb0dCAS |

Black, M., and Dixon, P. (1992) Stock identification and discrimination of mulloway in Australian waters. FIRTA (86/16): final report. The University of New South Wales, Sydney, NSW.

Caputi, N., Fletcher, W. J., Pearce, A., and Chubb, C. F. (1996). Effect of the Leeuwin Current on the recruitment of fish and invertebrates along the Western Australian coast. Marine and Freshwater Research 47, 147–155.
Effect of the Leeuwin Current on the recruitment of fish and invertebrates along the Western Australian coast.Crossref | GoogleScholarGoogle Scholar |

Cunningham, K. M., Canino, M. F., Spies, I. B., and Hauser, L. (2009). Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean. Canadian Journal of Fisheries and Aquatic Sciences 66, 153–166.
Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1antr8%3D&md5=421c2a6c9788f6140952ecdd96e6fa27CAS |

D’Anatro, A., Pereira, A. N., and Lessa, E. P. (2011). Genetic structure of the white croaker, Micropogonias furnieri Desmarest 1823 (Perciformes: Sciaenidae) along Uruguayan coasts: contrasting marine, estuarine, and lacustrine populations. Environmental Biology of Fishes 91, 407–420.
Genetic structure of the white croaker, Micropogonias furnieri Desmarest 1823 (Perciformes: Sciaenidae) along Uruguayan coasts: contrasting marine, estuarine, and lacustrine populations.Crossref | GoogleScholarGoogle Scholar |

Earl, D. A. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Earl, J., and Ward, T. M. (2014). Mulloway (Argyrosomus japonicus) stock assessment report 2013/14. Report to PIRSA Fisheries and Aquaculture, SARDI Publication number F2007/000898–3. SARDI Research Report Series number 814. South Australian Research and Development Institute (Aquatic Sciences), Adelaide, SA.

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=30e66402c232a6bc80a20ae0a1550038CAS | 15969739PubMed |

Excoffier, L., and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Farmer, B. M. (2008) Comparisons of the biological and genetic characteristics of the mulloway Argyosomus japonicus (Sciaenidae) in different regions of Western Australia. Ph.D. Thesis, Murdoch University, Perth, WA.

Ferguson, G. J. (2010) Impacts of river regulation, drought and exploitation on the fish in a degraded Australian estuary, with particular reference to the life-history of the sciaenid, Argyrosomus japonicus. Ph.D. Thesis, University of Adelaide, Adelaide, SA.

Ferguson, G. J., Ward, T. M., and Gillanders, B. M. (2011). Otolith shape and elemental composition: complimentary tools for stock discrimination of mulloway (Argyrosomus japonicus) in southern Australia. Fisheries Research 110, 75–83.
Otolith shape and elemental composition: complimentary tools for stock discrimination of mulloway (Argyrosomus japonicus) in southern Australia.Crossref | GoogleScholarGoogle Scholar |

Ferguson, G. J., Ward, T. M., Ivey, A., and Barnes, T. (2014). Life history of Argyrosomus japonicus, a large sciaenid at the southern part of its global distribution: implications for fisheries management. Fisheries Research 151, 148–157.
Life history of Argyrosomus japonicus, a large sciaenid at the southern part of its global distribution: implications for fisheries management.Crossref | GoogleScholarGoogle Scholar |

Gilbert, K. J., Andrew, R. L., Bock, D. G., Franklin, M. T., Kane, N. C., Moore, J. S., Moyers, B. T., Renaut, S., Rennison, D. J., and Veen, T. (2012). Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure. Molecular Ecology 21, 4925–4930.
Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure.Crossref | GoogleScholarGoogle Scholar | 22998190PubMed |

Gold, J., and Turner, T. (2002). Population structure of red drum (Sciaenops ocellatus) in the northern Gulf of Mexico, as inferred from variation in nuclear-encoded microsatellites. Marine Biology 140, 249–265.
Population structure of red drum (Sciaenops ocellatus) in the northern Gulf of Mexico, as inferred from variation in nuclear-encoded microsatellites.Crossref | GoogleScholarGoogle Scholar |

Goudet, J. (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3). Available at http://www2.unil.ch/popgen/softwares/fstat.htm [Verified 20 July 2015].

Griffiths, M. H. (1996). Life history of the dusky kob Argyrosomus japonicus (Sciaenidae) off the east coast of South Africa. South African Journal of Marine Science 17, 135–154.
Life history of the dusky kob Argyrosomus japonicus (Sciaenidae) off the east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |

Griffiths, M. H. (1997). The application of per-recruit models to Argyrosomus inodorus, an important South African sciaenid fish. Fisheries Research 30, 103–115.
The application of per-recruit models to Argyrosomus inodorus, an important South African sciaenid fish.Crossref | GoogleScholarGoogle Scholar |

Haffray, P., Malha, R., Ould Taleb Sidi, M., Prista, N., Hassan, M., Castelnaud, G., Karahan-Nomm, B., Gamsiz, K., Sadek, S., Bruant, J.-S., Balma, P., and Bonhomme, F. (2012). Very high genetic fragmentation in a large marine fish, the meagre Argyrosomus regius (Sciaenidae, Perciformes): impact of reproductive migration, oceanographic barriers and ecological factors. Aquatic Living Resources 25, 173–183.
Very high genetic fragmentation in a large marine fish, the meagre Argyrosomus regius (Sciaenidae, Perciformes): impact of reproductive migration, oceanographic barriers and ecological factors.Crossref | GoogleScholarGoogle Scholar |

Hall, D. A. (1986) An assessment of the mulloway (Argyrosomus hololepidotus) fishery in South Australia with particular reference to the Coorong Lagoon. Department of Fisheries Discussion Paper. South Australian Fisheries, Adelaide, SA.

Hayden, M. J., Nguyen, T., Waterman, A., McMichael, G., and Chalmers, K. J. (2008). Application of multiplex-ready PCR for fluorescence-based SSR genotyping in barley and wheat. Molecular Breeding 21, 271–281.
Application of multiplex-ready PCR for fluorescence-based SSR genotyping in barley and wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlyrs74%3D&md5=7ea8b5ab196c916031dc1731e996110dCAS |

Henry, G. W., and Lyle, J. M. (Eds) (2003) The national recreational and indigenous fishing survey. FAP Project FRDC Project number 99/158. Fisheries Research and Development Corporation, Canberra, ACT.

Hubisz, M. J., Falush, D., Stephens, M., and Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
Inferring weak population structure with the assistance of sample group information.Crossref | GoogleScholarGoogle Scholar | 21564903PubMed |

Jakobsson, M., and Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=67793b01e875d508b86e88f947314b6eCAS | 17485429PubMed |

Joseph, E. B. (1972). The status of the sciaenid stocks of the middle Atlantic coast. Chesapeake Science 13, 87–100.
The status of the sciaenid stocks of the middle Atlantic coast.Crossref | GoogleScholarGoogle Scholar |

Junge, C., Vøllestad, L. A., Barson, N. J., Haugen, T. O., Otero, J., Sætre, G. P., Leder, E. H., and Primmer, C. R. (2011). Strong gene flow and lack of stable population structure in the face of rapid adaptation to local temperature in a spring-spawning salmonid, the European grayling (Thymallus thymallus). Heredity 106, 460–471.
Strong gene flow and lack of stable population structure in the face of rapid adaptation to local temperature in a spring-spawning salmonid, the European grayling (Thymallus thymallus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7psFKjug%3D%3D&md5=6254ffd3dc63c1ee3b000b518c5e1bd7CAS | 21224882PubMed |

Klopper, A. W. (2011) Intraspecific genetic variation in the percoid teleosts Argyrosomus japonicus (Temminck & Schlegel, 1843) and Pomadasys commersonnii (Lacepède, 1801), as inferred from the mitochondrial control region. M.Sc.(Mar. Biol.) Thesis, University of Pretoria, Pretoria, South Africa.

Koizumi, I., Yamamoto, S., and Maekawa, K. (2006). Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr. Molecular Ecology 15, 3175–3189.
Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Shu7%2FP&md5=e5cd71b4eec9d171a8cb8a5018a1f505CAS | 16968263PubMed |

Lavergne, E., Calvès, I., Meistertzheim, A. L., Charrier, G., Zajonz, U., and Laroche, J. (2014). Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden. Marine Biology 161, 1113–1126.
Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXis1Cksbc%3D&md5=39b51cc019384d6754d927f926c47eaeCAS |

Nei, M. (1977). F‐statistics and analysis of gene diversity in subdivided populations. Annals of Human Genetics 41, 225–233.
F‐statistics and analysis of gene diversity in subdivided populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c%2FnvFWnsg%3D%3D&md5=c3f9a93627130c6a5c518bd1a4e6161dCAS | 596830PubMed |

O’Donnell, T., Denson, M., and Darden, T. (2014). Genetic population structure of spotted seatrout Cynoscion nebulosus along the south‐eastern USA. Journal of Fish Biology 85, 374–393.
Genetic population structure of spotted seatrout Cynoscion nebulosus along the south‐eastern USA.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjosVOntA%3D%3D&md5=683176c6273f97003e915808e27f2045CAS | 24890601PubMed |

O’Hara, T. D., and Poore, G. C. (2000). Patterns of distribution for southern Australian marine echinoderms and decapods. Journal of Biogeography 27, 1321–1335.
Patterns of distribution for southern Australian marine echinoderms and decapods.Crossref | GoogleScholarGoogle Scholar |

Ovenden, J. R. (2013). Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Marine and Freshwater Research 64, 201–207.
Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations.Crossref | GoogleScholarGoogle Scholar |

Ovenden, J. R., Kashiwagi, T., Broderick, D., Giles, J., and Salini, J. (2009). The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evolutionary Biology 9, 40.
The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago.Crossref | GoogleScholarGoogle Scholar | 19216767PubMed |

Petrusevics, P., Bye, J., Luick, J., and Teixeira, C. E. (2011). Summer sea surface temperature fronts and elevated chlorophyll-a in the entrance to Spencer Gulf, South Australia. Continental Shelf Research 31, 849–856.
Summer sea surface temperature fronts and elevated chlorophyll-a in the entrance to Spencer Gulf, South Australia.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=885f97093a81d621c8ba95f6e6f9f5f1CAS | 10835412PubMed |

Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
Analyzing tables of statistical tests.Crossref | GoogleScholarGoogle Scholar |

Rosenberg, N. A. (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
DISTRUCT: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |

Rousset, F. (2008). GENEPOP’007: a complete re‐implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
GENEPOP’007: a complete re‐implementation of the GENEPOP software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar | 21585727PubMed |

Ryman, N., and Palm, S. (2006). POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes 6, 600–602.
POWSIM: a computer program for assessing statistical power when testing for genetic differentiation.Crossref | GoogleScholarGoogle Scholar |

Shaddick, K., Gilligan, D. M., Burridge, C. P., Jerry, D. R., Truong, K., and Beheregaray, L. B. (2011). Historic divergence with contemporary connectivity in a catadromous fish, the estuary perch (Macquaria colonorum). Canadian Journal of Fisheries and Aquatic Sciences 68, 304–318.
Historic divergence with contemporary connectivity in a catadromous fish, the estuary perch (Macquaria colonorum).Crossref | GoogleScholarGoogle Scholar |

Taylor, M. D., and Piola, R. F. (2008). Scale stocking checks to differentiate between hatchery-reared and wild mulloway Argyrosomus japonicus. Fisheries Management and Ecology 15, 211–216.
Scale stocking checks to differentiate between hatchery-reared and wild mulloway Argyrosomus japonicus.Crossref | GoogleScholarGoogle Scholar |

Taylor, M. D., Laffan, S. D., Fielder, D. S., and Suthers, I. M. (2006). Key habitat and home range of mulloway Argyrosomus japonicus in a south-east Australian estuary: finding the estuarine niche to optimise stocking. Marine Ecology Progress Series 328, 237–247.
Key habitat and home range of mulloway Argyrosomus japonicus in a south-east Australian estuary: finding the estuarine niche to optimise stocking.Crossref | GoogleScholarGoogle Scholar |

Taylor, M. D., van der Meulen, D. E., Ives, M. C., Walsh, C. T., Reinfelds, I. V., and Gray, C. A. (2014). Shock, stress or signal? Implications of freshwater flows for a top-level estuarine predator. PLoS One 9, e95680.
Shock, stress or signal? Implications of freshwater flows for a top-level estuarine predator.Crossref | GoogleScholarGoogle Scholar | 24752585PubMed |

Ward, R. D., and Elliott, N. G. (2001). Genetic population structure of species in the South East Fishery of Australia. Marine and Freshwater Research 52, 563–573.
Genetic population structure of species in the South East Fishery of Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVaqtLc%3D&md5=b8b571b8bd9858517721797a02c53d78CAS |

Waters, J. M. (2008). Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Diversity & Distributions 14, 692–700.
Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both?Crossref | GoogleScholarGoogle Scholar |

Watts, R. J., and Johnson, M. S. (2004). Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Marine and Freshwater Research 55, 641–651.
Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes.Crossref | GoogleScholarGoogle Scholar |

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Whitfield, A. K., and Cowley, P. D. (2010). The status of fish conservation in South African estuaries. Journal of Fish Biology 76, 2067–2089.
The status of fish conservation in South African estuaries.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3crhtlegug%3D%3D&md5=b06ac42fa164917788e49a2d4058a686CAS | 20557655PubMed |