Population genetic structure of barramundi (Lates calcarifer) across the natural distribution range in Australia informs fishery management and aquaculture practices
Shannon R. Loughnan A , Carolyn Smith-Keune B , Luciano B. Beheregaray A , Nicholas A. Robinson C D and Dean R. Jerry B E FA College of Science and Engineering, Flinders University, PO Box 2100, Adelaide, SA 5001, Australia.
B Centre for Sustainable Tropical Fisheries and Aquaculture, College of Science and Engineering, James Cook University, Townsville, Qld 4811, Australia.
C Nofima, PO Box 5010, N-1432 Ås, Norway.
D Sustainable Aquaculture Laboratory – Temperate and Tropical (SALTT), School of BioSciences, The University of Melbourne, Vic 3010, Australia.
E Tropical Futures Institute, James Cook University, 149 Sims Drive, 387380, Singapore.
F Corresponding author. Email: dean.jerry@jcu.edu.au
Marine and Freshwater Research 70(11) 1533-1542 https://doi.org/10.1071/MF18330
Submitted: 2 September 2018 Accepted: 23 March 2019 Published: 31 May 2019
Abstract
Clarifying population structure of fish stocks is important for the sustainable exploitation of fisheries, along with informing collection of founder broodstock for the genetic improvement of aquaculture programs. Using 16 microsatellite DNA markers, the most comprehensive genetic survey to date (1297 individuals from 49 sample collections) of the population structure and genetic diversity of wild Australian barramundi (Lates calcarifer) was undertaken. The results point to the existence of two distinct genetic stocks (east and west) with isolation by geographic distance (IBD), and a central region of admixture between the stocks, located in an area where a historic land bridge once connected northern Australia with Papua New Guinea. Global levels of population differentiation were moderate (fixation index, FST = 0.103, P < 0.001) and IBD was identified as a factor influencing population structure across the sampled region. There was also evidence of temporal stability of population genetic structure over a period of 25 years. This study provides valuable information for improving programs of translocation, restocking and captive breeding for both the wild barramundi fishery and the aquaculture industry.
Additional keywords: Asian seabass, connectivity, genetic diversity, microsatellite.
References
Adamkewicz, S. L., and Harasewych, M. G. (1996). Systematics and biogeography of the genus Donax (Bivalvia: Donacidae) in eastern North America. American Malacological Bulletin 13, 97–103.Attard, C. R. M., Möller, L. M., Sasaki, M., Hammer, M. P., Bice, C., Brauer, C., Carvalho, D., Harris, J., and Beheregaray, L. B. (2016). A novel holistic framework for genetic-based captive breeding and reintroduction programs. Conservation Biology Journal 30, 1060–1069.
| A novel holistic framework for genetic-based captive breeding and reintroduction programs.Crossref | GoogleScholarGoogle Scholar |
Beheregaray, L. B., Ciofi, C., Caccone, A., Gibbs, J. P., and Powell, J. R. (2003). Genetic divergence, phylogeography and conservation units of giant tortoises from Santa Cruz and Pinzón, Galápagos Islands. Conservation Biology Journal 4, 31–46.
| Genetic divergence, phylogeography and conservation units of giant tortoises from Santa Cruz and Pinzón, Galápagos Islands.Crossref | GoogleScholarGoogle Scholar |
Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B. Methodological 57, 289–300.
| Controlling the false discovery rate: a practical and powerful approach to multiple testing.Crossref | GoogleScholarGoogle Scholar |
Chenoweth, S. F., Hughes, J. M., Keenan, C. P., and Lavery, S. (1998a). Concordance between dispersal and mitochondrial gene flow: isolation by distance in a tropical teleost, Lates calcarifer (Australian barramundi). Heredity 80, 187–197.
| Concordance between dispersal and mitochondrial gene flow: isolation by distance in a tropical teleost, Lates calcarifer (Australian barramundi).Crossref | GoogleScholarGoogle Scholar |
Chenoweth, S. F., Hughes, J. M., Keenan, C. P., and Lavery, S. (1998b). When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface. Proceedings of the Royal Society of London – B. Biological Sciences 265, 415–420.
| When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface.Crossref | GoogleScholarGoogle Scholar |
Cross, T. F. (2000). Genetic implications of translocation and stocking of fish species, with particular reference to Western Australia. Aquaculture Research 31, 83–94.
| Genetic implications of translocation and stocking of fish species, with particular reference to Western Australia.Crossref | GoogleScholarGoogle Scholar |
Davis, T. L. O. (1986). Migration patterns in barramundi, Lates calcarifer (Bloch), in Van Diemen Gulf, Australia, with estimates of fishing mortality in specific areas. Fisheries Research 4, 243–258.
| Migration patterns in barramundi, Lates calcarifer (Bloch), in Van Diemen Gulf, Australia, with estimates of fishing mortality in specific areas.Crossref | GoogleScholarGoogle Scholar |
Dethmers, K. E. M., Broderick, D., Moritz, C., Fitzsimmons, N. N., Limpus, C. J., Lavery, S., Whiting, S., Guinea, M., Prince, R. I. T., and Kennett, R. (2006). The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Molecular Ecology 15, 3931–3946.
| The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange.Crossref | GoogleScholarGoogle Scholar |
Doupé, R. G., Horwitz, P., and Lymbery, A. J. (1999). Mitochondrial genealogy of Western Australian barramundi: applications of inbreeding coefficients and coalescent analysis for separating temporal population processes. Journal of Fish Biology 54, 1197–1209.
| Mitochondrial genealogy of Western Australian barramundi: applications of inbreeding coefficients and coalescent analysis for separating temporal population processes.Crossref | GoogleScholarGoogle Scholar |
Duncan, K. M., Martin, A. P., Bowen, B. W., and de Couet, H. G. (2006). Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology 15, 2239–2251.
| Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini).Crossref | GoogleScholarGoogle Scholar | 16780437PubMed |
Earl, D. A., and vanHoldt, B. M. (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 |
Edmunds, R. C., van Herwerden, L., and Fulton, C. J. (2010). Population-specific locomotor phenotypes are displayed by barramundi, Lates calcarifer, in response to thermal stress. Canadian Journal of Fisheries and Aquatic Sciences 67, 1068–1074.
| Population-specific locomotor phenotypes are displayed by barramundi, Lates calcarifer, in response to thermal stress.Crossref | GoogleScholarGoogle Scholar |
Eknath, A. E., Tayamen, M. M., Palada-de Vera, M. S., Danting, J. C., Reyes, R. A., Dionisio, E. E., Capili, J. B., Bolivar, H. L., Abella, T. A., Circa, A. V., Bentsen, H. B., Gjerde, B., Gjedrem, T., and Pullin, R. S. V. (1993). Genetic improvement of farmed tilapias: the growth performance of eight strains of Oreochromis niloticus tested in different farm environments. Aquaculture 111, 171–188.
| Genetic improvement of farmed tilapias: the growth performance of eight strains of Oreochromis niloticus tested in different farm environments.Crossref | GoogleScholarGoogle Scholar |
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 | 15969739PubMed |
Excoffier, L., Laval, L. G., and Schneider, S. (2005). ARLEQUIN (Version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| ARLEQUIN (Version 3.0): an integrated software package for population genetics data analysis.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., Veen, T., and Vines, T. H. (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 |
Gjedrem, T., Gjøen, H. M., and Gjerde, B. (1991). Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98, 41–50.
| Genetic origin of Norwegian farmed Atlantic salmon.Crossref | GoogleScholarGoogle Scholar |
Grey, D. L. (1986). An overview of Lates calcarifer in Australia and Asia. In ‘Management of Wild and Cultured Sea Bass/Barramundi (Lates calcarifer): Proceedings of an International Workshop’, 24–30 September 1986, Darwin, NT, Australia. (Eds J. W. Copland and D. L. Grey.) pp. 15–21. (Canberra Publishing & Printing Co.: Canberra, ACT, Australia.)
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 | 17485429PubMed |
Jerry, D. R., and Smith-Keune, C. (2014). The genetics of Asian seabass. In ‘Biology and Culture of Asian Seabass Lates calcarifer’. (Ed. D. R. Jerry.) pp. 137–177. (CRC Press: Boca Raton, FL, USA.)
Jombart, T. (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
| adegenet: a R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar | 18397895PubMed |
Jombart, T., and Ahmed, I. (2011). adegenet 1.3–1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071.
| adegenet 1.3–1: new tools for the analysis of genome-wide SNP data.Crossref | GoogleScholarGoogle Scholar | 21926124PubMed |
Kalinowski, S. T. (2005). HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5, 187–189.
| HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness.Crossref | GoogleScholarGoogle Scholar |
Keenan, C. P. (1994). Recent evolution of population structure in Australian barramundi, Lates calcarifer (Bloch): an example of isolation by distance in one dimension. Marine and Freshwater Research 45, 1123–1148.
| Recent evolution of population structure in Australian barramundi, Lates calcarifer (Bloch): an example of isolation by distance in one dimension.Crossref | GoogleScholarGoogle Scholar |
Keenan, C. P. (2000). Should we allow human-induced migration of the Indo-West Pacific fish, barramundi Lates calcarifer (Bloch) within Australia? Aquaculture Research 31, 121–131.
| Should we allow human-induced migration of the Indo-West Pacific fish, barramundi Lates calcarifer (Bloch) within Australia?Crossref | GoogleScholarGoogle Scholar |
Loughnan, S. R., Domingos, J. A., Smith-Keune, C., Forrester, J. P., Jerry, D. R., Beheregaray, L. B., and Robinson, N. A. (2013). Broodstock contribution after mass spawning and size grading in barramundi (Lates calcarifer, Bloch). Aquaculture 404–405, 139–149.
| Broodstock contribution after mass spawning and size grading in barramundi (Lates calcarifer, Bloch).Crossref | GoogleScholarGoogle Scholar |
Loughnan, S. R., Smith-Keune, C., Jerry, D. R., Beheregaray, L. B., and Robinson, N. A. (2016). Genetic diversity and relatedness estimates for captive barramundi (Lates calcarifer, Bloch) broodstock populations informs efforts to form a base population for selective breeding. Aquaculture Research 47, 3570–3584.
| Genetic diversity and relatedness estimates for captive barramundi (Lates calcarifer, Bloch) broodstock populations informs efforts to form a base population for selective breeding.Crossref | GoogleScholarGoogle Scholar |
Marshall, C. R. E. (2005). Evolutionary genetics of barramundi (Lates calcarifer) in the Australian region. Ph.D. Thesis, Murdoch University, Perth, WA, Australia.
Meirmans, P. G. (2012). The trouble with isolation by distance. Molecular Ecology 21, 2839–2846.
| The trouble with isolation by distance.Crossref | GoogleScholarGoogle Scholar | 22574758PubMed |
Meirmans, P. G., and Van Tienderen, P. H. (2004). GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4, 792–794.
| GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms.Crossref | GoogleScholarGoogle Scholar |
Mirams, A. G. K., Treml, E. A., Shields, J. L., Liggins, L., and Riginos, C. (2011). Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge. Coral Reefs 30, 937–949.
| Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge.Crossref | GoogleScholarGoogle Scholar |
Moore, R. (1982). Spawning and early life history of barramundi, Lates calcarifer (Bloch), in Papua New Guinea. Marine and Freshwater Research 33, 647–661.
| Spawning and early life history of barramundi, Lates calcarifer (Bloch), in Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |
Moore, R., and Reynolds, L. F. (1982). Migration patterns of barramundi, Lates calcarifer (Bloch), in Papua New Guinea. Marine and Freshwater Research 33, 671–682.
| Migration patterns of barramundi, Lates calcarifer (Bloch), in Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |
Newton, J. R., Smith-Keune, C., and Jerry, D. R. (2010). Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation. Aquaculture 308, S128–S132.
| Thermal tolerance varies in tropical and sub-tropical populations of barramundi (Lates calcarifer) consistent with local adaptation.Crossref | GoogleScholarGoogle Scholar |
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 10835412PubMed |
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 |
Salini, J., and Shaklee, J. B. (1987). Barramundi discoveries may change management. Australian Fisheries 46, 2–6.
Salini, J., and Shaklee, J. B. (1988). Genetic structure of barramundi (Lates calcarifer) stocks from northern Australia. Marine and Freshwater Research 39, 317–329.
| Genetic structure of barramundi (Lates calcarifer) stocks from northern Australia.Crossref | GoogleScholarGoogle Scholar |
Saunders, T., Whybird, O., Trinnie, F., and Newman, S. (2016). Barramundi (2018) Lates calcarifer. In ‘Status of Australian Fish Stocks Reports 2016’. (Fisheries Research and Development Corporation: Canberra, ACT, Australia.) Available at http://fish.gov.au/report/204-Barramundi-2018 [Verified 22 April 2019].
Shaklee, J. B., and Salini, J. P. (1983). Studies suggest multiple stocks of Australian barramundi. Australian Fisheries 42, 36–38.
Shaklee, J. B., and Salini, J. P. (1985). Genetic variation and population subdivision in Australian barramundi, Lates calcarifer (Bloch). Marine and Freshwater Research 36, 203–218.
| Genetic variation and population subdivision in Australian barramundi, Lates calcarifer (Bloch).Crossref | GoogleScholarGoogle Scholar |
Shaklee, J. B., Salini, J., and Garrett, R. N. (1993). Electrophoretic characterization of multiple genetic stocks of barramundi perch in Queensland, Australia. Transactions of the American Fisheries Society 122, 685–701.
| Electrophoretic characterization of multiple genetic stocks of barramundi perch in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Unmack, P. J. (2001). Biogeography of Australian freshwater fishes. Journal of Biogeography 28, 1053–1089.
| Biogeography of Australian freshwater fishes.Crossref | GoogleScholarGoogle Scholar |
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 |
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 | 28563791PubMed |
Yue, G. H., Zhu, Z. Y., Lo, L. C., Wang, C. M., Lin, G., Feng, F., Pang, H. Y., Li, J., Gong, P., Liu, H. M., Tan, J., Chou, R., Lim, H., and Orban, L. (2009). Genetic variation and population structure of Asian seabass (Lates calcarifer) in the Asia-Pacific region. Aquaculture 293, 22–28.
| Genetic variation and population structure of Asian seabass (Lates calcarifer) in the Asia-Pacific region.Crossref | GoogleScholarGoogle Scholar |