Skip to main content
SpringerLink
Log in

Developing a genetic baseline for the yellowtail amberjack species complex, Seriola lalandi sensu lato, to assess and preserve variation in wild populations of these globally important aquaculture species

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Recent study suggest the globally distributed yellowtail amberjack, Seriola lalandi sensu lato, is a complex of three closely related species. Together, these and three other species of Seriola comprise an important component of global aquaculture production with an estimated annual value of $1.3 billion. As yellowtail aquaculture grows, the impact of unintentional releases on wild populations has become an increasingly important issue, particularly in light of international trade of hatchery seed. To create a genetic baseline, we examined spatial genetic structure in 260 specimens collected from seven locations over a wide geographical range using 15 nuclear microsatellites and mitochondrial control region sequences. Overall genetic differentiation among locations, as revealed by microsatellite data, was highly significant (FST = 0.085, DEST = 0.382, P < 0.001), and pairwise estimates of divergence derived from mitochondrial and microsatellite data support the presence of four significantly differentiated populations corresponding to the N.E. Pacific, N.W. Pacific, S. Pacific, and South Atlantic. Based on the genetic differentiation detected in this study, and recently published sequence data, these populations more accurately reflect the presence of at least three cryptic species of Seriola. Especially strong genetic differentiation between hemispheres indicates that the equatorial region is a significant dispersal barrier for yellowtail. This study represents the broadest geographic investigation of genetic population structure conducted, to date, for specimens of the S. lalandi complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Baskett ML, Waples RS (2013) Evaluating alternative strategies for minimizing unintended fitness consequences of cultured individuals on wild populations. Conserv Biol 27:83–94

    Article  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, Logiciel Sous Windows TM Pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier

  • Bourret V, O’reilly PT, Carr JW, Berg PR, Bernatchez L (2011) Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees. Heredity 106:500–510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Coombs JA, Letcher BH, Nislow KH (2008) CREATE: a software to create input files from diploid genotypic data for 52 genetic software programs. Mol Ecol Res 8:578–580

    Article  CAS  Google Scholar 

  • Danancher D, Garcia-Vazquez E (2011) Genetic population structure in flatfishes and potential impact of aquaculture and stock enhancement on wild populations in Europe. Rev Fish Biol Fish 21:441–462

    Article  Google Scholar 

  • Dann TH, Smoker WW, Hard JJ, Gharrett AJ (2010) Outbreeding depression after two generations of hybridizing southeast Alaska coho salmon populations? Trans Am Fish Soc 139:1292–1305

    Article  Google Scholar 

  • Díaz-Jaimes P, Uribe-Alcocer M (2006) Spatial differentiation in the eastern Pacific yellowfin tuna revealed by microsatellite variation. Fish Sci 72:590–596

    Article  Google Scholar 

  • Drummond, AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A (2009) Geneious v4.7. http://www.geneious.com

  • Dunn K (2014) The diet, reproductive biology, age and growth of yellowtail, Seriola lalandi, in South Africa. Master thesis, University of Cape Town, Cape Town. pp 106

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Edmands S (2002) Does parental divergence predict reproductive compatibility? Trends Ecol Evol 17:520–527

    Article  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Erisman B, Mascarenas I, Paredes G, Sadovy de Mitcheson Y, Aburto-Oropeza O, Hastings P (2010) Seasonal, annual, and long-term trends in commercial fisheries for aggregating reef fishes in the Gulf of California, Mexico. Fish Res 106:279–288

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

  • FAO (2012) The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations, Rome, p 209

    Google Scholar 

  • Fielder DS, Heasman MP (2011) Hatchery manual for the production of Australian bass, mulloway and yellowtail kingfish. New South Wales Department of Industry and Investment Fisheries and Research Development Corporation, Taylors Beach, p 170

    Google Scholar 

  • Fraser DJ, Houde AL, Debes PV, O’Reilly P, Eddington JD, Hutchings JA (2010) Consequences of farmed-wild hybridization across divergent wild populations and multiple traits in salmon. Ecol Appl 20:935–953

    Article  PubMed  Google Scholar 

  • Gauthier DT, Audemard CA, Carlsson JEL, Darden TL, Denson MR, Reece KS, Carlsson J (2013) Genetic population structure of US Atlantic coastal striped bass (Morone saxatilis). J Hered 104:510–520

    Article  CAS  PubMed  Google Scholar 

  • Glover KA, Quintela M, Wennevik V, Besnier F, Sørvik AG, Skaala Ø (2012) Three decades of farmed escapees in the wild: a spatio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS One 7:e43129

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goudet J (2002) FSTAT 2.9.3.2, a program to estimate and test gene diversities and fixation indices. http://www.unil.ch/izea/softwates/fstat.html

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hansen MM, Olivieri I, Waller DM, Nielsen EE (2012) Monitoring adaptive genetic responses to environmental change. Mol Ecol 21:1311–1329

    Article  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Hutchings JA, Fraser DJ (2008) The nature of fisheries-and farming-induced evolution. Mol Ecol 17:294–313

    Article  PubMed  Google Scholar 

  • Hutchings JA, Swain DP, Rowe S, Eddington JD, Puvanendran V, Brown JA (2007) Genetic variation in life-history reaction norms in a marine fish. Proc Biol Sci 274:1693–1699

    Article  PubMed Central  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6, 13. v.3.23 http://ibdws.sdsu.edu/

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper ML (2006) ML-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    Article  CAS  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lorenzen K, Beveridge M, Mangel M (2012) Cultured fish: integrative biology and management of domestication and interactions with wild fish. Biol Rev Camb Philos Soc 87:639–660

    Article  PubMed  Google Scholar 

  • Martinez-Takeshita N, Purcell CM, Chabot CL, Craig MT, Paterson CN, Hyde JR, Allen LG (2015) A tale of three tails: cryptic speciation in a globally distributed marine fish of the genus Seriola. Copeia 103:357–368

    Article  Google Scholar 

  • Mehner T, Pohlmann K, Elkin C, Monaghan MT, Freyhof J (2009) Genetic mixing from enhancement stocking in commercially exploited vendace populations. J Appl Ecol 46:1340–1349

    Google Scholar 

  • Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Res. doi:10.1111/1755-0998.12216

    Google Scholar 

  • Miller PA, Fitch AJ, Gardner M, Hutson KS, Mair G (2011) Genetic population structure of Yellowtail Kingfish (Seriola lalandi) in temperate Australasian waters inferred from microsatellite markers and mitochondrial DNA. Aquaculture 319:328–336

    Article  CAS  Google Scholar 

  • Moen T, Hayes B, Nilsen F, Delghandi M, Fjalestad KT, Fevolden SE, Berg PR, Lien S (2008) Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genet 9:18

    Article  PubMed Central  PubMed  Google Scholar 

  • Moran D, Smith CK, Gara B, Poortenaar CW (2007) Reproductive behavior and early development in yellowtail kingfish (Seriola lalandi Valenciennes 1833). Aquaculture 262:95–104

    Article  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009a) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150

    Article  PubMed  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Poulsen NA, Loeschcke V, Moen T, Johansen T, Mittelholzer C, Taranger GL, Ogden R, Carvalho GR (2009b) Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol Biol 9:276

    Article  PubMed Central  PubMed  Google Scholar 

  • Nugroho E, Taniguchi N (1999) Isolation of greater amberjack microsatellite DNA and their application as genetic marker to species of genus Seriola from Japan. Fish Sci 65:353–357

    CAS  Google Scholar 

  • Nugroho E, Ferrell DJ, Smith P, Taniguchi N (2001) Genetic divergence of kingfish from Japan, Australia and New Zealand inferred by microsatellite DNA and mitochondrial DNA control region markers. Fish Sci 67:843–850

    Article  CAS  Google Scholar 

  • Ohara E, Nishimura T, Sakamoto T, Nagakura Y, Mushiake K, Okamoto N (2003) Isolation and characterization of microsatellite loci from yellowtail Seriola quinqueradiata and cross-species amplification within the genus Seriola. Mol Ecol Notes 3:390–391

  • Ohara E, Nishimura T, Nagakura Y, Sakamoto T, Mushiake K, Okamoto N (2005) Genetic linkage maps of two yellowtails (Seriola quinqueradiata and Seriola lalandi). Aquaculture 244:41–48

  • Ozaki A, Yoshida K, Fuji K, Kubota S, Kai W, Aoki J, Kawabata Y, Suzuki J, Akita K, Koyama T, Nakagawa M, Hotta T, Tsuzaki T, Okamoto N, Araki K, Sakamoto T (2013) Quantitative Trait Loci (QTL) associated with resistance to a monogenean parasite (Benedenia seriolae) in yellowtail (Seriola quinqueradiata) through genome wide analysis. PLOS One 8:e64987

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20

    Article  Google Scholar 

  • Porta JM, Novel P, Martinez-Rodriguez G, Alvarez MC, Porta J (2009) Isolation and characterization of microsatellites from Seriola dumerili (Risso 1810). Aqua Res 40:249–251

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Poulsen NA, Hemmer-Hansen J, Loeschcke V, Carvalho GR, Nielsen EE (2011) Microgeographical population structure and adaptation in Atlantic cod Gadus morhua: spatio-temporal insights from gene-associated DNA markers. Mar Ecol Prog Ser 436:231–243

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pusack TJ, Christie MR, Johnson DW, Stallings CD, Hixon MA (2014) Spatial and temporal patterns of larval dispersal in a coral-reef fish metapopulation: evidence of variable reproductive success. Mol Ecol 23:3396–3408

    Article  PubMed  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Renshaw MA, Patton JC, Rexroad CE, Gold JR (2006) PCR primers for trinucleotide and tetranucleotide microsatellites in greater amberjack, Seriola dumerili. Mol Ecol Notes 6:1162–1164

    Article  CAS  Google Scholar 

  • Renshaw MA, Patton JC, Rexroad CE, Gold JR (2007) Isolation and characterization of dinucleotide microsatellites in greater amberjack, Seriola dumerili. Conserv Genet 8:1009–1011

    Article  CAS  Google Scholar 

  • Rice W (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Sala E, Aburto-Oropeza O, Paredes G, Thompson G (2003) Spawning aggregations and reproductive behavior of reef fishes in the Gulf of California. Bull Mar Sci 72:103–121

    Google Scholar 

  • Shiraishi T, Ohshimo S, Yukami R (2010) Age, growth and reproductive characteristics of gold striped amberjack 1 Seriola lalandi in the waters off western Kyushu, Japan. N Z J Mar Fresh Res 44:117–127

    Article  CAS  Google Scholar 

  • Sumida BY, Moser HG, Ahlstrom E (1985) Descriptions of larvae of California yellowtail, Seriola lalandi, and three other carangids from the eastern tropical Pacific: Chloroscombrus orquna, Caranx caballus, and Caranx sexfasciatus. CalCofi Rep 26:139–159

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Theisen TC, Bowen BW, Baldwin JD (2008) High connectivity on a global scale in the pelagic wahoo, Acanthocybium solandri (tuna family Scombridae). Mol Ecol 17:4233–4247

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Utter F, Epifanio J (2002) Marine aquaculture: genetic potentialities and pitfalls. Rev Fish Biol Fish 12:59–77

    Article  Google Scholar 

  • Viñas J, Alvarado Bremer JR, Pla C (2004) Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Mar Biol 145:225–232

    Article  Google Scholar 

  • Wahlund S (1928) Zusammensetzun von Populationen und Korrelation-sersheininungen von Standpunkt der Verebungslehre aus betrachtet. Hereditas 11:65–106

    Article  Google Scholar 

  • Waples RS, Hindar K, Hard JJ (2012) Genetic risks associated with marine aquaculture. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-NWFSC-119, p 149

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed Central  PubMed  Google Scholar 

  • Zimmermann EW, Purchase CF, Fleming IA, Brattey J (2013) Dispersal of wild and escapee farmed Atlantic cod (Gadus morhua) in Newfoundland. Can J Fish Aquat Sci 70:747–755

    Article  Google Scholar 

Download references

Acknowledgments

For specimen collection, the authors thank M. Steele, FV Toronado, FV Aloha Spirit, FV Cobra, RV Yellowfin, FV Royal Polaris, FV Pursuit, FV Earl Grey, Naigai Foods, Inc. (Fukuoka, Kyushu, Japan), Dr. K. Saitoh of the National Research Institute of Fisheries Science (Aquatic Genomics Research Center) in Tokyo, Japan, Museo Nacional de Historia Natural, Gobierno de Chile, R. Roodt-Wilding’s Laboratory at Stellenbosch University, various pangas, and private sport and commercial fishermen. Specimens in CA were collected using permit #000032 and #SC12372 from the California Department of Fish and Game. The authors thank D. Kacev, M. Lauf, M. Sherman, who provided technical and analytical assistance.

Funding

Funding for this study was provided by the National Institute of Health, Minority Biomedical Research Support Research Initiative for Scientific Enhancement program (NIH MBRS RISE) (#2R25GM063787), M. Takeshita, the Nearshore Marine Fish Research Program, Department of Biology, California State University, Northridge, the National Research Council Postdoctoral Fellowship program, and the US National Marine Fisheries Service.

Author information

Authors and Affiliations

  1. National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Southwest Fisheries Science Center, 8901 La Jolla Shores Dr., La Jolla, CA, 92037, USA

    Catherine M. Purcell, Matthew T. Craig & John R. Hyde

  2. Department of Biology, California State University, Northridge, CA, 91330-8303, USA

    Chris L. Chabot, Natalie Martinez-Takeshita & Larry G. Allen

Authors
  1. Catherine M. Purcell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris L. Chabot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew T. Craig
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Natalie Martinez-Takeshita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Larry G. Allen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John R. Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catherine M. Purcell.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals

Tissue specimens used in this study were collected from dead fish that had been previously captured by commercial and recreational fisheries using standard ethical angling practices under California Department of Fish and Wildlife Scientific Collecting Permit #SC12372 and #000032, from museum archives, and international fishery research agencies.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1494 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Purcell, C.M., Chabot, C.L., Craig, M.T. et al. Developing a genetic baseline for the yellowtail amberjack species complex, Seriola lalandi sensu lato, to assess and preserve variation in wild populations of these globally important aquaculture species. Conserv Genet 16, 1475–1488 (2015). https://doi.org/10.1007/s10592-015-0755-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0755-8

Keywords

Search

Navigation