Skip to main content
SpringerLink
Log in

Demographic Expansion and Subtle Differentiation in the Long-Tailed Hake Macruronus magellanicus: Evidence from Microsatellite Data

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The impact of geographic heterogeneity and historical demographic factors on genetic diversity in the commercially exploited hake Macruronus magellanicus was examined applying microsatellite markers. A total of 450 fish from 6 different sites, collected in Atlantic Patagonia, were genotyped at 6 polymorphic loci. While analysis of variance-based methods (Fst-Rst) failed to detect differentiation, the exact test for genic differentiation and factorial correspondence analysis revealed subtle differences between coastal and continental shelf edge samples. Data suggest that M. magellanicus has been subjected to a demographic expansion 2.6 to 5 times its original size thatoccurred approximately 100,000 to 200,000 years ago. Another more recent expansion seems to have occurred a few generations ago. Implications of subtle structuring and demographic instability are discussed.

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

  • DG Altman (1991) Practical Statistics for Medical Research Chapman & Hall London

    Google Scholar 

  • B Angers L Bernatchez (1998) ArticleTitleCombined use of SMM and non-SMM methods to infer fine structure and evolutionary history of closely related brook charr (Salvelinus fontinalis Salmonidae) populations from microsatellies Mol Biol Evol 15 143–159

    Google Scholar 

  • E Arnason (2004) ArticleTitleMitochondrial cytochrome b DNA variation in the high-fecundity Atlantic cod: trans-atlantic clines and shallow gene genealogy Genetics 166 1871–1885 Occurrence Handle10.1534/genetics.166.4.1871

    Article  Google Scholar 

  • F Balloux N Lugon-Moulin (2002) ArticleTitleThe estimation of population differentiation with microsatellite markers Mol Ecol 11 155–165

    Google Scholar 

  • F Balloux H Brunner N Lugon-Moulin J Hausser J Goudet (2000) ArticleTitleMicrosatellites can be misleading: An empirical and simulation study Evolution 54 1414–1422

    Google Scholar 

  • TD Beacham DE Hay KD Le (2005) ArticleTitlePopulation structure and stock identification of eulachon (Thaleichthys pacificus), an anadromous smelt, in the Pacific northwest Mar Biotechnol 7 363–372 Occurrence Handle10.1007/s10126-004-4075-0

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme, F (2002) GENETIX 4.03, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier (France). Available from http://www.univ-montp2.fr/~genetix/genetix/genetix.htm

  • LW Botsford JC Castilla (1997) ArticleTitleThe management of fisheries and marine ecosystems Science 277 509–515 Occurrence Handle10.1126/science.277.5325.509

    Article  Google Scholar 

  • AGF Castillo JL Martínez E Garcia-Vazquez (2004) ArticleTitleFine spatial structure of atlantic hake (Merluccius merluccius) stocks revealed by variation at microsatellite loci Mar Biotechnol 6 299–306 Occurrence Handle10.1007/s10126-004-3027-z

    Article  Google Scholar 

  • R Chakraborty M Andrade ParticleDe SP Daiger B Budowle (1992) ArticleTitleApparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications Ann Hum Genet 56 45–57

    Google Scholar 

  • D Corach (1991) ArticleTitleA reliable, rapid and simple method for DNA extraction from frozen sperm cells Fingerprint News 3 13

    Google Scholar 

  • JM Cornuet G Luikart (1996) ArticleTitleDescription and power analysis of two tests for detecting recent population bottlenecks from allele frequency data Genetics 144 2001–2014

    Google Scholar 

  • JM Cornuet G Luikart (1998) ArticleTitleEmpirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data Conserv Biol 12 228–237

    Google Scholar 

  • ME D'Amato GR Carvalho (2005) ArticleTitlePopulation genetic structure and history of the long-tailed hake, Macruronus magellanicus, in the SW Atlantic as revealed by mtDNA RFLP analysis Ices J Mar Sci 62 247–265

    Google Scholar 

  • ME D'Amato DH Lunt GR Carvalho (1999) ArticleTitleMicrosatellite markers for the hake Macruronus magellanicus amplify other gadoids Mol Ecol 8 1086–1088 Occurrence Handle10.1046/j.1365-294X.1999.00655_7.x

    Article  Google Scholar 

  • JA DeWoody JC Avise (2000) ArticleTitleMicrosatellite variation in marine, freshwater and anadromous fishes compared with other animals J Fish Biol 56 461–473 Occurrence Handle10.1111/j.1095-8649.2000.tb00748.x

    Article  Google Scholar 

  • A Mousadik ParticleEl RJ Petit (1996) ArticleTitleHigh level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L) Skeels] endemic to Morocco Theor Appl Genet 92 832–839

    Google Scholar 

  • A Estoup B Angers (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations GR Carvalho (Eds) Advances in Molecular Ecology IOP Press Amsterdam 56–86

    Google Scholar 

  • A Estoup P Jarne JM Cornuet (2002) ArticleTitleHomoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis Mol Ecol 11 1591–1604 Occurrence Handle10.1046/j.1365-294X.2002.01576.x

    Article  Google Scholar 

  • OE Gaggiotti O Lange K Rassman C Gliddons (1999) ArticleTitleA comparison of two indirect methods for estimating average levels of gene flow using microsatellite data Mol Ecol 8 1513–1520 Occurrence Handle10.1046/j.1365-294x.1999.00730.x

    Article  Google Scholar 

  • F Garoia I Guarniero C Piccinetti F Tinti (2004) ArticleTitleFirst microsatellite loci of red mullet (Mullus barbatus) and their application to genetic structure analysis of Adriatic shared stock Mar Biotechnol 6 446–452 Occurrence Handle10.1007/s10126-004-3045-x

    Article  Google Scholar 

  • Giussi AR (1996) Estudio de algunos aspectos del ciclo vital de la merluza de cola Macruronus magellanicus, Lönnberg, 1907. Tesis Doctoral. Universidad Nacional de Mar del Plata

  • Giussi AR, Hernández D, Abachian V (1999) Differences in growth of long tailed hake (Macruronus magellanicus) from two areas of South-western Atlantic ocean. In: Avances en Métodos y Tecnología aplicados a la Investigación Pesquera. Seminario final del Proyecto INIDEP-JICA sobre Evaluación y Monitoreo de Recursos Pesqueros 1994–1999. Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Mar del Plata, Argentina, pp 131–134

  • SJ Goodman (1997) ArticleTitleA collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance Mol Ecol 6 881–885 Occurrence Handle10.1046/j.1365-294X.1997.00260.x

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Update from Goudet 1995. Available from http://www.unil.ch/izea/softwares/fstat.html

  • WS Grant BW Bowen (1998) ArticleTitleShallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation J Hered 89 415–426

    Google Scholar 

  • JE Graves (1998) ArticleTitleMolecular insights into population structure of cosmopolitan fishes J Hered 89 427–437 Occurrence Handle10.1093/jhered/89.5.427

    Article  Google Scholar 

  • B Guinand (1996) ArticleTitleUse of a multivariate model using allele frequency distributions to analyse patterns of genetic differentiation among populations Biol J Linn Soc 58 173–195 Occurrence Handle10.1006/bijl.1996.0031

    Article  Google Scholar 

  • SW Guo EA Thompson (1992) ArticleTitlePerforming the Exact Test of Hardy-Weinberg proportions for multiple alleles Biometrics 48 361–372

    Google Scholar 

  • B Hanfling B Hellemans FAM Volckaert GR Carvalho (2002) ArticleTitleLate glacial history of the cold-adapted freshwater fish Cottus gobio, revealed by microsatellites Mol Ecol 11 1717–1729 Occurrence Handle10.1046/j.1365-294X.2002.01563.x

    Article  Google Scholar 

  • L Hauser RD Ward (1998) Population identification in pelagic fish: the limits of molecular markers GR Carvalho (Eds) Advances in Molecular Ecology IOS Press Amsterdam 191–224

    Google Scholar 

  • WF Hutchinson GR Carvalho SI Rogers (2001) ArticleTitleMarked genetic structuring in localised spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites Mar Ecol Prog Ser 223 251–260

    Google Scholar 

  • ST Kalinowski (2002a) ArticleTitleHow many alleles per locus should be used to estimate genetic distances? Heredity 88 62–65 Occurrence Handle10.1038/sj.hdy.6800009

    Article  Google Scholar 

  • ST Kalinowski (2002b) ArticleTitleEvolutionary and statistical properties of three genetic distances Mol Ecol 11 1263–1273 Occurrence Handle10.1046/j.1365-294X.2002.01520.x

    Article  Google Scholar 

  • H Knutsen PE Jorde C André NC Stenseth (2003) ArticleTitleFine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod Mol Ecol 12 385–394 Occurrence Handle10.1046/j.1365-294X.2003.01750.x

    Article  Google Scholar 

  • G Luikart FW Allendorf JM Cornuet WB Sherwin (1998) ArticleTitleDistortion of allele frequency distributions provides a test for recent population bottlenecks J Hered 89 238–247 Occurrence Handle10.1093/jhered/89.3.238

    Article  Google Scholar 

  • CJ Lundy P Moran C Rico RS Milner GM Hewitt (1999) ArticleTitleMacrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius), a commercially important fish Mol Ecol 8 1889–1898 Occurrence Handle10.1046/j.1365-294x.1999.00789.x

    Article  Google Scholar 

  • CJ Lundy C Rico GM Hewitt (2000) ArticleTitleTemporal and spatial genetic variation in spawning grounds of European hake (Merluccius merluccius) in the Bay of Biscay Mol Ecol 9 2067–2079 Occurrence Handle10.1046/j.1365-294X.2000.01120.x

    Article  Google Scholar 

  • M Nei (1987) Molecular Evolutionary Genetics Columbia University Press New York

    Google Scholar 

  • R Nielsen (1997) ArticleTitleA maximum likelihood approach to population samples of microsatellite alleles Genetics 146 711–716

    Google Scholar 

  • PT O'Reilly MF Canino KM Bailey P Bentzen (2004) ArticleTitleInverse relationship between Fst and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure Mol Ecol 13 1799–1814 Occurrence Handle10.1111/j.1365-294X.2004.02214.x

    Article  Google Scholar 

  • SR Palumbi (1994) ArticleTitleGenetic divergence, reproductive isolation and marine speciation Annu Rev Ecol Syst 25 522–547 Occurrence Handle10.1146/annurev.es.25.110194.002555

    Article  Google Scholar 

  • Perier MR, Di Giácomo EE (1999) La merluza de cola en la pesquería del Golfo San Matías: un recurso alternativo. In: Avances en Métodos y Tecnología Aplicados a la Investigación Pesquera. Seminario Final del Proyecto INIDEP-JICA Sobre Evaluación y Monitoreo de Recursos Pesqueros (1994–1999), pp 209–211

  • S Piry G Luikart JM Cornuet (1999) ArticleTitleBOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data J Hered 90 502–503 Occurrence Handle10.1093/jhered/90.4.502

    Article  Google Scholar 

  • DM Rand (1996) ArticleTitleNeutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology Conserv Biol 10 665–671 Occurrence Handle10.1046/j.1523-1739.1996.10020665.x

    Article  Google Scholar 

  • M Raymond F Rousset (1995) ArticleTitleAn Exact Test for population differentiation Evolution 49 1280–1283

    Google Scholar 

  • M Raymond F Rousset (1997) ArticleTitleGENEPOP (version 3.3): population genetics software for Exact Tests an ecumenicism Updated version of J Hered 86 248–249

    Google Scholar 

  • WR Rice (1989) ArticleTitleAnalyzing tables of statistical tests Evolution 43 223–225

    Google Scholar 

  • F Rousset M Raymond (1995) ArticleTitleTesting heterozygote excess and deficiency Genetics 140 1413–1419

    Google Scholar 

  • DE Ruzzante CT Taggart D Cook S Goddard (1996) ArticleTitleGenetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: microsatellite variation and antifreeze level Can J Fish Aquat Sci 53 634–645

    Google Scholar 

  • DE Ruzzante CT Taggart D Cook (1998) ArticleTitleA nuclear basis for shelf- and bank-scale population structure in northwest Atlantic cod (Gadus morhua): Labrador to Georges Bank. Mol Ecol 7 1663–1680 Occurrence Handle10.1046/j.1365-294x.1998.00497.x

    Article  Google Scholar 

  • DE Ruzzante CT Taggart D Cook (1999) ArticleTitleA review of the evidence for genetic structure of cod (Gadus morhua) populations in the NW Atlantic and population affinities of larval cod off Newfoundland and the Gulf of St. Lawrence Fish Res 43 79–97 Occurrence Handle10.1016/S0165-7836(99)00067-3

    Article  Google Scholar 

  • N Ryman F Utter L Laikre (1995) ArticleTitleProtection of intraspecific biodiversity of exploited species Rev Fish Biol Fish 5 417–446

    Google Scholar 

  • J Sambrook JEF Fritsch T Maniatis (1989) Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  • M Sekino M Hara (2001) ArticleTitleApplication of microsatellite markers to population genetics studies of Japanese flounder Paralichthys olivaceus Mar Biotechnol 3 572–589

    Google Scholar 

  • PW Shaw GJ Pierce PR Boyle (1999a) ArticleTitleSubtle population structuring within a vagile marine invertebrate, the veneid squid Loligo forbesi, demonstrated with microsatellite markers Mol Ecol 8 407–417 Occurrence Handle10.1046/j.1365-294X.1999.00588.x

    Article  Google Scholar 

  • PW Shaw C Turan JM Wright M O'Connell GR Carvalho (1999b) ArticleTitleMicrosatellite DNA analysis of population structure in Atlantic herring Clupea harengus, with direct comparison to allozyme and mtDNA data Heredity 83 490–499 Occurrence Handle10.1038/sj.hdy.6885860

    Article  Google Scholar 

  • MD Shriver L Jin RE Ferrell R Deka (1997) ArticleTitleMicrosatellite data supports an early population expansion in Africa Genome Res 7 586–591

    Google Scholar 

  • M Slatkin (1995) ArticleTitleA measure of population subdivision based on microsatellite allele frequencies Genetics 139 1463

    Google Scholar 

  • EE Sotka JA Hempelmann CH Biermann (2005) ArticleTitleGenetic evidence of postglacial population expansion in Puget Sound rockfish (Sebastes emphaeus) Mar Biotechnol 7 223–230 Occurrence Handle10.1007/s10126-004-0437-x

    Article  Google Scholar 

  • J Stabile JR Waldman F Parauka W Wirgin (1996) ArticleTitleStock structure and homing fidelity in Gulf of Mexico Sturgeon (Acipenser oxyrinchus desotoi) based on restriction fragment length polymorphism and sequence analysis of mitochondrial DNA Genetics 144 767–775

    Google Scholar 

  • RL Stephenson (1999) ArticleTitleStock complexity in fisheries management: a perspective of emerging issues related to population sub-units Fish Res 43 247–249 Occurrence Handle10.1016/S0165-7836(99)00076-4

    Article  Google Scholar 

  • MJH Oppen ParticleVan C Rico JC Deutsch GF Turner GM Hewitt (1997) ArticleTitleIsolation and characterization of microsatellite loci in the cichlid fish Pseudotropeus zebra Mol Ecol 6 387–388

    Google Scholar 

  • RS Waples (1998) ArticleTitleSeparating the wheat from the chaff: patterns of genetic differentiation in high gene flow species J Hered 98 438–450

    Google Scholar 

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

    Google Scholar 

  • Wöhler, O.C., Hansen, J.E., Giussi, A.R., Cordo, H.D. (2001). Tendencia de la abundancia de la merluza de cola(Macruronus magellanicus) en el Atlántico Sudoccidental durante el período 1985–2000 y recomendaciones de la captura biológicamente acceptable correspondienteal año 2001. Informe Técnico Interno INIDEP N° 15, 11 pp.

    Google Scholar 

Download references

Acknowledgments

I am indebted to Dr. Bruno Prenski (formerly Instituto Nacional de Investigación y Desarrollo Pesquero), Daniel Corach (Universidad de Buenos Aires), Fernando Dulout (Universidad Nacional de La Plata), Marta Lizarralde, (Centro Austral de Investigaciones Científicas), Lorenzo Lamatina (Universidad de Mar del Plata), and Atila Gostonyi (Centro Nacional Patagónico) for access to their lab facilities for DNA extraction prior to the starting of the fellowship; to Alejandro Pettovello (Centro de Investigaciones Puerto Deseado), Raúl González (Instituto de Biología Marina y Pesquera Almte. Storni), Gustavo Lovrich (Centro Austral de Investigaciones Científicas), Joost Pompert, Connor Nolan (Falkland Islands Government Fisheries Department), and Bruno Prenski, for collection of samples; to Martin Donnelly (Liverpool School of Tropical Medicine) for helpful discussions on data analysis and specially to Professor Gary Carvalho (University of Wales) for the discussions on the results and critically reading of the manuscript.

Author information

Author notes

  1. María Eugenia D'Amato

    Present address: Biodiversity and Conservation Biology Department, University of the Western Cape, Private Bag X17, 7535, Bellville, South Africa

Authors and Affiliations

  1. Department of Biological Sciences, University of Hull, Hull, HU6 7RX, United Kingdom

    María Eugenia D'Amato

  2. Consejo Nacional de Investigaciones Científicas (CONICET), Argentina

    María Eugenia D'Amato

Authors
  1. María Eugenia D'Amato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Eugenia D'Amato.

Rights and permissions

Reprints and permissions

About this article

Cite this article

D'Amato, M.E. Demographic Expansion and Subtle Differentiation in the Long-Tailed Hake Macruronus magellanicus: Evidence from Microsatellite Data. Mar Biotechnol 8, 189–201 (2006). https://doi.org/10.1007/s10126-005-5075-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-005-5075-4

Keywords

Search

Navigation