Spatial genetic subdivision among populations of the highly migratory black marlin Istiompax indica within the central Indo-Pacific
Samuel M. Williams A B E , Michael B. Bennett B , Julian G. Pepperell D , Jess A. T. Morgan A D and Jennifer R. Ovenden A B
+ Author Affiliations
- Author Affiliations
A Molecular Fisheries Laboratory, The University of Queensland, St Lucia, Qld 4072, Australia.
B School of Biomedical Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.
C Pepperell Research and Consulting Pty Ltd, PO Box 1475, Noosaville DC, Qld 4566, Australia.
D Queensland Alliance for Agriculture and Food Innovation, the University of Queensland, St Lucia, Qld 4069, Australia.
E Corresponding author. Email: samuel.williams5@uq.net.au
Marine and Freshwater Research 67(8) 1205-1214 https://doi.org/10.1071/MF14370
Submitted: 18 November 2014 Accepted: 20 April 2015 Published: 7 September 2015
Abstract
The black marlin Istiompax indica is a highly migratory species and as a result is expected to show little genetic population structure throughout its broad geographic range. Tissue samples from 183 I. indica were collected from three geographic regions within the central Indo-Pacific and analysed using mitochondrial and nuclear DNA markers. Nuclear genetic heterogeneity was found among populations in the south-western Pacific Ocean, eastern Indian Ocean and South China Sea (significant FST values of 0.013–0.037). Combining information from nuclear markers with published movement and reproductive data suggests that reproductive philopatry plays a role in maintaining contemporary I. indica population structure. Analyses of the mitochondrial control region did not reflect this pattern; however, it identified historical population structure. Differing patterns of genetic population structure revealed by mitochondrial and nuclear markers demonstrated that a transition must have occurred between historical and contemporary population structures. This restructuring presumably reflects a species whose populations have become genetically isolated before experiencing a period of secondary contact. The spatial subdivision evident among populations indicates that I. indica in this central Indo-Pacific region should be managed as three independent stocks, to guide the sustainability of this fisheries resource.
Additional keywords: billfish, citizen science, fisheries management, philopatry, population structure.
References
Alvarado Bremer, J. R., Viñas, J., Mejuto, J., Ely, B., and Pla, C. (2005). Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Molecular Phylogenetics and Evolution 36, 169–187.| Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1Oiurc%3D&md5=2606b28582b7839cc2fb11ee3f6f4509CAS | 15904864PubMed |
Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., and Wheeler, D. L. (2003). GenBank. Nucleic Acids Research 31, 23–27.
| GenBank.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFSgu78%3D&md5=b0dbe113118f6d13b073162f25ac34ccCAS | 12519940PubMed |
Blower, D. C., Pandolfi, J. M., Bruce, B. D., Gomez-Cabrera, M., and Ovenden, J. R. (2012). Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes. Marine Ecology Progress Series 455, 229–244.
| Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Sht77I&md5=3a64f59dba7c5a273a17ab3d8353247eCAS |
Buonaccorsi, V., McDowell, J., and Graves, J. (2001). Reconciling patterns of inter‐ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Molecular Ecology 10, 1179–1196.
| Reconciling patterns of inter‐ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktFKitbY%3D&md5=ea926e682e0ed54d35242093e2b2ecb9CAS | 11380876PubMed |
Carlsson, J., McDowell, J. R., Diaz-Jaimes, P., Carlsson, J. E., Boles, S. B., Gold, J. R., and Graves, J. E. (2004). Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus) population structure in the Mediterranean Sea. Molecular Ecology 13, 3345–3356.
| Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus) population structure in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWkurjM&md5=dde0d84446268ad2076e8b3ac1937e14CAS | 15487994PubMed |
Carlsson, J., McDowell, J. R., Carlsson, J. E. L., and Graves, J. E. (2007). Genetic identity of YOY bluefin tuna from the eastern and Western Atlantic spawning areas. The Journal of Heredity 98, 23–28.
| Genetic identity of YOY bluefin tuna from the eastern and Western Atlantic spawning areas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Wnt7s%3D&md5=0fca70cab9a37370024368bb4e2c92edCAS | 17158466PubMed |
Chiang, H.-C., Hsu, C.-C., Lin, H.-D., Ma, G. C., Chiang, T.-Y., and Yang, H.-Y. (2006). Population structure of bigeye tuna (Thunnus obesus) in the South China Sea, Philippine Sea and western Pacific Ocean inferred from mitochondrial DNA. Fisheries Research 79, 219–225.
| Population structure of bigeye tuna (Thunnus obesus) in the South China Sea, Philippine Sea and western Pacific Ocean inferred from mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Chiang, W.-C., Musyl, M. K., Sun, C.-L., DiNardo, G., Hung, H.-M., Lin, H.-C., Chen, S.-C., Yeh, S.-Z., Chen, W.-Y., and Kuo, C.-L. (2015). Seasonal movements and diving behavior of black marlin (Istiompax indica) in the northwestern Pacific Ocean. Fisheries Research 166, 92–102.
| Seasonal movements and diving behavior of black marlin (Istiompax indica) in the northwestern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Collette, B. B., McDowell, J. R., and Graves, J. E. (2006). Phylogeny of recent billfishes (Xiphioidei). Bulletin of Marine Science 79, 455–468.
Collette, B., Acero, A., Canales Ramirez, C., Carpenter, K. E., Di Natale, A., Fox, W., Miyabe, N., Montano Cruz, R., Nelson, R., Schaefer, K., Serra, R., Sun, C., Uozumi, Y., and Yanez, E. (2011a). Istiompax indica (Black Marlin). In ‘IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2’. (International Union for Conservation of Nature and Natural Resources.) Available at http://www.iucnredlist.org/details/170312/0 [Verified 23 June 2015].
Collette, B. B., Carpenter, K. E., Polidoro, B. A., Juan-Jordá, M. J., Boustany, A., Die, D. J., Elfes, C., Fox, W., Graves, J., Harrison, L. R., McManus, R., Minte-Vera, C. V., Nelson, R., Restrepo, V., Schratwieser, J., Sun, C.-L., Amorim, A., Brick Peres, M., Canales, C., Cardenas, G., Chang, S.-K., Chiang, W.-C., de Oliveira Leite, N., Harwell, H., Lessa, R., Fredou, F. L., Oxenford, H. A., Serra, R., Shao, K.-T., Sumaila, R., Wang, S.-P., Watson, R., and Yáñez, E. (2011b). High value and long life – double jeopardy for tunas and billfishes. Science 333, 291–292.
| High value and long life – double jeopardy for tunas and billfishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps1Kisbs%3D&md5=3d9640401d4b067f6af6627b0df02f60CAS | 21737699PubMed |
Domeier, M. L., and Speare, P. (2012). Dispersal of adult black marlin (Istiompax indica) from a Great Barrier Reef spawning aggregation. PLoS One 7, e31629.
| Dispersal of adult black marlin (Istiompax indica) from a Great Barrier Reef spawning aggregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVeisL4%3D&md5=f41d5ade0e25d9fb8258154184b77da2CAS | 22363692PubMed |
Durand, J.-D., Collet, A., Chow, S., Guinand, B., and Borsa, P. (2005). Nuclear and mitochondrial DNA markers indicate unidirectional gene flow of Indo-Pacific to Atlantic bigeye tuna (Thunnus obesus) populations, and their admixture off southern Africa. Marine Biology 147, 313–322.
| Nuclear and mitochondrial DNA markers indicate unidirectional gene flow of Indo-Pacific to Atlantic bigeye tuna (Thunnus obesus) populations, and their admixture off southern Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVClu70%3D&md5=3744efacedc5d983749a7058e3ffda10CAS |
Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=42d24496932e9475cc1dbfe8f1382286CAS |
Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| 1:CAS:528:DC%2BD3sXnvF2ntrk%3D&md5=d2d80f182068d08c2b15265debc7276fCAS | 12930761PubMed |
Funk, D. J., and Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics 34, 397–423.
| Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Galtier, N., Nabholz, B., Glémin, S., and Hurst, G. (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18, 4541–4550.
| Mitochondrial DNA as a marker of molecular diversity: a reappraisal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1SjsL%2FM&md5=2e1049867d8f2b2a90de6397ac6af41fCAS | 19821901PubMed |
Gorbunova, N. N. (1976). The classification and distribution of the larvae of Indo-Pacific species of billfishes from the family Istiophoridae. Journal of Ichthyology 16, 437–451.
Graves, J. E. (1998). Molecular insights into the population structures of cosmopolitan marine fishes. The Journal of Heredity 89, 427–437.
| Molecular insights into the population structures of cosmopolitan marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFCjtbc%3D&md5=138ea4a075841c512a4fb12897717d1bCAS |
Graves, J. E., and McDowell, J. R. (1995). Inter-ocean genetic divergence of istiophorid billfishes. Marine Biology 122, 193–203.
Graves, J. E., and McDowell, J. R. (2003). Stock structure of the world’s istiophorid billfishes: a genetic perspective. Marine and Freshwater Research 54, 287–298.
| Stock structure of the world’s istiophorid billfishes: a genetic perspective.Crossref | GoogleScholarGoogle Scholar |
Gunn, J. S., Patterson, T. A., and Pepperell, J. G. (2003). Short-term movement and behaviour of black marlin Makaira indica in the Coral Sea as determined through a pop-up satellite archival tagging experiment. Marine and Freshwater Research 54, 515–525.
| Short-term movement and behaviour of black marlin Makaira indica in the Coral Sea as determined through a pop-up satellite archival tagging experiment.Crossref | GoogleScholarGoogle Scholar |
Hellberg, M. E., Burton, R. S., Neigel, J. E., and Palumbi, S. R. (2002). Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70, 273–290.
Hokkaido University (1980). Data record of oceanographic observations and exploratory fishing, number 23. The Faculty of Fisheries, Hokkaido University, Hakodate, Japan.
Holland, K. N. (2003). A perspective on billfish biological research and recommendations for the future. Marine and Freshwater Research 54, 343–347.
| A perspective on billfish biological research and recommendations for the future.Crossref | GoogleScholarGoogle Scholar |
Hudson, R. R., and Turelli, M. (2003). Stochasticity overrules the ‘three‐times rule’: genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution 57, 182–190.
| 12643581PubMed |
Jones, S., and Kumaran, M. (1964). Distribution of larval billfishes (Xiphiidae and Istiophoridae) in the Indo-Pacific with special reference to the collections made by the Danish Dana expedition. In ‘Proceedings of the Symposium on Scombroid Fishes’, 12–15 January 1962, Mandapam Camp, India. Symposium Series 1, pp. 499–528. (Marine Biological Association of India: Cochin, Kerala, India.)
Kopf, R. K., Davie, P. S., Bromhead, D. B., and Young, J. W. (2012). Reproductive biology and spatiotemporal patterns of spawning in striped marlin Kajikia audax. Journal of Fish Biology 81, 1834–1858.
| Reproductive biology and spatiotemporal patterns of spawning in striped marlin Kajikia audax.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s3ltFahuw%3D%3D&md5=06cf9fd4e762562a4dd47abccde1cee3CAS | 23130686PubMed |
Latch, E., Dharmarajan, G., Glaubitz, J., and Rhodes, O. (2006). Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics 7, 295–302.
| Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation.Crossref | GoogleScholarGoogle Scholar |
Latch, E. K., Reding, D. M., Heffelfinger, J. R., Alcalá-Galván, C. H., and Rhodes, O. E. (2014). Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography. Molecular Ecology 23, 3171–3190.
| Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography.Crossref | GoogleScholarGoogle Scholar | 24863151PubMed |
Leis, J., Goldman, B., and Ueyanagi, S. (1987). Distribution and abundance of billfish larvae (Pisces: Istiophoridae) in the Great Barrier Reef lagoon and Coral Sea near Lizard Island, Australia. Fishery Bulletin 85, 757–765.
McDowell, J. R. (2002). Genetic stock structure of the sailfish, Istiophorus platypterus, based on nuclear and mitochondrial DNA. Ph.D. thesis, The College of William and Mary, Williamsburg, VA, USA.
McDowell, J. R., and Graves, J. E. (2008). Population structure of striped marlin (Kajikia audax) in the Pacific Ocean based on analysis of microsatellite and mitochondrial DNA. Canadian Journal of Fisheries and Aquatic Sciences 65, 1307–1320.
| Population structure of striped marlin (Kajikia audax) in the Pacific Ocean based on analysis of microsatellite and mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1KgsL4%3D&md5=c468ea33c9da2a9ad2ebe5f78961d63cCAS |
Muths, D., Le Couls, S., Evano, H., Grewe, P., and Bourjea, J. (2013). Multi-genetic marker approach and spatio-temporal analysis suggest there is a single panmictic population of swordfish Xiphias gladius in the Indian Ocean. PLoS One 8, e63558.
| Multi-genetic marker approach and spatio-temporal analysis suggest there is a single panmictic population of swordfish Xiphias gladius in the Indian Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVGlurg%3D&md5=956bf5e7424eb50761a4bb5562a916b8CAS | 23717447PubMed |
Nakadate, M., Vinas, J., Corriero, A., Clarke, S., Suzuki, N., and Chow, S. (2005). Genetic isolation between Atlantic and Mediterranean albacore populations inferred from mitochondrial and nuclear DNA markers. Journal of Fish Biology 66, 1545–1557.
| Genetic isolation between Atlantic and Mediterranean albacore populations inferred from mitochondrial and nuclear DNA markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFOgs7k%3D&md5=39385e0dbeaf81e9ccf16920120cc31fCAS |
Nakamura, I. (1975). Synopsis of the biology of the black marlin, Makaira indica (Cuvier), 1831. In ‘Proceedings of the International Billfish Symposium’, 9–12 August 1972, Kailua-Kona, HI, USA. Part 3 Species Synopses (Eds R. S. Shomura and F. S. Williams.) NOAA Technical Report. NMFS. Special Scientific Report-Fisheries Series (675) Part 3, pp. 17–27. (National Marine Fisheries Service; Seattle, WA, USA.)
Nakamura, I. (1985). ‘FAO Species Catalogue. v. 5: Billfishes of the World. An Annotated and Illustrated Catalogue of Marlins, Sailfishes, Spearfishes and Swordfishes Known to Date.’ (United Nations Development Program, Food and Agriculture Organization: Rome.)
Ortiz, M., Prince, E. D., Serafy, J. E., Holts, D. B., Davy, K. B., Pepperell, J. G., Lowry, M. B., and Holdsworth, J. C. (2003). Global overview of the major constituent-based billfish tagging programs and their results since 1954. Marine and Freshwater Research 54, 489–507.
| Global overview of the major constituent-based billfish tagging programs and their results since 1954.Crossref | GoogleScholarGoogle Scholar |
Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=9ffa44a19aa460f6905d8dc9e4ab7a43CAS | 22820204PubMed |
Peel, E., Nelson, R., and Goodyear, C. P. (2003). Managing Atlantic marlin as bycatch under ICCAT. The fork in the road: recovery or collapse. Marine and Freshwater Research 54, 575–584.
| Managing Atlantic marlin as bycatch under ICCAT. The fork in the road: recovery or collapse.Crossref | GoogleScholarGoogle Scholar |
Pepperell, J. G. (1990). Movements and variations in early year-class strength of black marlin (Makaira indica) off eastern Australia. In ‘Proceedings of the Second International Billfish Symposium’, 1–5 August 1988, Kailua-Kona, HI, USA. (Ed. R. H. Stroud.) Part 2, pp. 51–66. (National Coalition for Marine Conservation: Savannah, GA.)
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 |
Purcell, C. M., and Edmands, S. (2011). Resolving the genetic structure of striped marlin, Kajikia audax, in the Pacific Ocean through spatial and temporal sampling of adult and immature fish. Canadian Journal of Fisheries and Aquatic Sciences 68, 1861–1875.
| Resolving the genetic structure of striped marlin, Kajikia audax, in the Pacific Ocean through spatial and temporal sampling of adult and immature fish.Crossref | GoogleScholarGoogle Scholar |
Reiss, H., Hoarau, G., Dickey-Collas, M., and Wolff, W. J. (2009). Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish and Fisheries 10, 361–395.
| Genetic population structure of marine fish: mismatch between biological and fisheries management units.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=3c6e97fae4013ea47a8ead7e83fa3f79CAS | 12912839PubMed |
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 |
Selkoe, K. A., and Toonen, R. J. (2006). Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9, 615–629.
| Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers.Crossref | GoogleScholarGoogle Scholar | 16643306PubMed |
Skillman, R. A. (1990). Status of Pacific billfish stocks. In ‘Proceedings of the Second International Billfish Symposium’, 1–5 August 1988, Kailua-Kona, HI, USA. (Ed. R. H. Stroud.) Part 1, pp. 179–95. (National Coalition for Marine Conservation: Savannah, GA.)
Speare, P. (1992). A technique for tetracycline injecting and tagging billfish. Bulletin of Marine Science 51, 197–203.
Speare, P. (1994). Relationships among the black marlin, Makaira indica, in eastern Australian coastal waters, inferred from parasites Australian Journal of Marine and Freshwater Research 45, 535–549.
| Relationships among the black marlin, Makaira indica, in eastern Australian coastal waters, inferred from parasitesCrossref | GoogleScholarGoogle Scholar |
Speare, P. (1999). Parasites from east-coast Australian billfish. Memoirs of the Queensland Museum 43, 837–848.
Speare, P. (2003). Age and growth of black marlin, Makaira indica, in east coast Australian waters. Marine and Freshwater Research 54, 307–314.
| Age and growth of black marlin, Makaira indica, in east coast Australian waters.Crossref | GoogleScholarGoogle Scholar |
Sulaiman, Z. H., and Ovenden, J. R. (2010). Population genetic evidence for the east–west division of the narrow-barred Spanish mackerel (Scomberomorus commerson, Perciformes: Teleostei) along Wallace’s Line. Biodiversity and Conservation 19, 563–574.
| Population genetic evidence for the east–west division of the narrow-barred Spanish mackerel (Scomberomorus commerson, Perciformes: Teleostei) along Wallace’s Line.Crossref | GoogleScholarGoogle Scholar |
Sun, C.-L., Chang, H.-Y., Liu, T.-Y., and Yeh, S.-Z. (2015). Reproductive biology of black marlin, Istiompax indica, off southwestern and eastern Taiwan. Fisheries Research 166, 12–20.
| Reproductive biology of black marlin, Istiompax indica, off southwestern and eastern Taiwan.Crossref | GoogleScholarGoogle Scholar |
Takagi, M., Okamura, T., Chow, S., and Taniguchi, N. (2001). Preliminary study of albacore (Thunnus alalunga) stock differentiation inferred from microsatellite DNA analysis. Fishery Bulletin 99, 697–701.
Toews, D. P., and Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 3907–3930.
| The biogeography of mitochondrial and nuclear discordance in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Cgt7rE&md5=31c75df8c067552ccf7ef428358c8d7bCAS | 22738314PubMed |
Ueyanagi, S. (1962). Description and distribution of larvae of five istiphorid species in the Indo-Pacific. In ‘Proceedings of the Symposium on Scombroid Fishes’, 12–15 January 1962, Mandapam Camp, India. Symposium Series 1, pp. 499–528. (Marine Biological Association of India: Cochin, Kerala, India.)
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P., 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 |
Waples, R. (1998). Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. The Journal of Heredity 89, 438–450.
| Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species.Crossref | GoogleScholarGoogle Scholar |
Waples, R. S., and Gaggiotti, O. (2006). INVITED REVIEW: what is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology 15, 1419–1439.
| INVITED REVIEW: what is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVCjur4%3D&md5=be5ac36a5db16a55faa80860c37c692fCAS | 16629801PubMed |
Ward, R. (2000). Genetics in fisheries management. Hydrobiologia 420, 191–201.
| Genetics in fisheries management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlSktLc%3D&md5=c00739a3c7a5e2b7ccbac0c2acf27f7cCAS |
Ward, R., Woodwark, M., and Skibinski, D. (1994). A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. Journal of Fish Biology 44, 213–232.
| A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes.Crossref | GoogleScholarGoogle Scholar |
Ward, R. D., Reeb, C. A., Block, B. A., and Grove, P. (2001). Population structure of Australian swordfish, Xiphias gladius. Final Report to the Australian Fisheries Management Authority, Canberra.
Williams, S. M., Pepperell, J. G., Corley, S. W., and Ovenden, J. R. (2015a). Isolation and characterisation of 18 polymorphic microsatellite loci for black marlin (Istiompax indica) and their utility for Pacific billfish species. Fisheries Research 166, 29–32.
| Isolation and characterisation of 18 polymorphic microsatellite loci for black marlin (Istiompax indica) and their utility for Pacific billfish species.Crossref | GoogleScholarGoogle Scholar |
Williams, S. M., Morgan, J. A., and Ovenden, J. R. (2015b). The complete validated mitochondrial genome of the black marlin Istiompax indica (Cuvier, 1832). Mitochondrial DNA , .
| The complete validated mitochondrial genome of the black marlin Istiompax indica (Cuvier, 1832).Crossref | GoogleScholarGoogle Scholar |
Wu, G. C.-C., Chiang, H.-C., Chen, K.-S., Hsu, C.-C., and Yang, H.-Y. (2009). Population structure of albacore (Thunnus alalunga) in the Northwestern Pacific Ocean inferred from mitochondrial DNA. Fisheries Research 95, 125–131.
| Population structure of albacore (Thunnus alalunga) in the Northwestern Pacific Ocean inferred from mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
