Scientia Marina, Vol 77, No 4 (2013)

Searching for a stock structure in Sardina pilchardus from the Adriatic and Ionian seas using a microsatellite DNA-based approach


https://doi.org/10.3989/scimar.03843.26A

Paolo Ruggeri
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche , Italy

Andrea Splendiani
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche , Italy

Sara Bonanomi
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche - Technical University of Denmark, National Institute of Aquatic Resources, Section for Marine Living , Italy

Enrico Arneri
FAO-FIRF, Fisheries and Aquaculture Department, AdriaMed Project , Italy

Nando Cingolani
Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima , Italy

Alberto Santojanni
Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima , Italy

Sabrina Colella
Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima , Italy

Fortunata Donato
Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima , Italy

Massimo Giovannotti
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche , Italy

Vincenzo Caputo Barucchi
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche - Consiglio Nazionale delle Ricerche, Istituto di Scienze Marine Sezione Pesca Marittima , Italy

Abstract


In the present study the genetic variability of European sardine from Adriatic and Ionian seas was investigated in order to detect the occurrence of genetic structure within and between these basins. In several samples the analysis of genetic variability at eight microsatellite loci showed a number of homozygote individuals higher than expected at Hardy-Weinberg equilibrium. The inter-population differentiation level estimated by AMOVA, qST and rRST and Bayesian descriptors detected no signs of population differentiation between the samples analysed. These results are consistent with previous studies based on allozymes and several mitochondrial DNA markers and add further evidence contradicting the early identification, based on morphological and reproductive data, of two sub-populations in the Adriatic Sea.

Keywords


microsatellite DNA; population genetics; European sardine; stock identification method; small pelagic fish; Adriatic Sea; Ionian Sea

Full Text:


PDF

References


Abaunza P., Murta A.G., Campbell N., Cimmaruta R., Comesana A.S., Dahle G., Santamaria M.T.G., Gordo L.S., Iversen S.A., MacKenzie K., Magoulas A., Mattiucci S., Molloy J., Nascetti G., Pinto A.L., Quinta R., Rarnos P., Sanjuan A., Santos A.T., Stransky C., Zimmermann C. 2008. Stock identity of horse mackerel (Trachurus trachurus) in the northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches. Fisher. Res. 89: 196-209. http://dx.doi.org/10.1016/j.fishres.2007.09.022

Alegrìa-Hernàndez V., Jardas I., Sinovčić G. 1986. Observations on the differences between sardine, Sardina pilchardus (Walb.) subpopulations from the eastern Adriatic. FAO Fisheries Report 345, pp. 137-160.

André C., Larsson L.C., Laikre L., Bekkevold D., Brigham J., Carvalho G.R., Dahlgren T.G., Hutchinson W.F., Mariani S., Mudde K., Ruzzante D.E., Ryman N. 2011. Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity 106: 270-280. http://dx.doi.org/10.1038/hdy.2010.71

Artegiani A., Bregant D., Paschini E., Pinardi N., Raicich F., Russo A. 1997. The Adriatic Sea general circulation. Part I: air-sea interactions and water mass structure. J. Physic. Ocean. 27: 1492-1514. http://dx.doi.org/10.1175/1520-0485(1997)027<1492:TASGCP>2.0.CO;2

Atarhouch T., Ru.ber L., Gonzalez E.G., Albert E.M., Rami M., Dakkak A., Zardoya R. 2006. Signature of an early genetic bottleneck in a population of Moroccan sardines (Sardina pilchardus). Mol. Phyl. Evol. 39: 373-383. http://dx.doi.org/10.1016/j.ympev.2005.08.003

Baibai T., Oukhattar L., Vasquez Quinteiro J., Mesfioui A., Rey-Mendez M., Soukri A. 2012. First global approach: morphological and biological variability in a genetically homogeneous population of the European pilchard, Sardina pilchardus (Walbaum, 1792) in the North Atlantic coast. Rev. Fish Biol. Fish. 22(1): 63-80. http://dx.doi.org/10.1007/s11160-011-9223-9

Beaumont M.A., Nichols R.A. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lon. Ser. B-Biol. Sci. 263: 1619-1626.

Beaumont M.A. 2002. FDIST2. Available from http://rubic.rdg.ac.uk/Bmab/software.html.

Begg G.A., Waldman J.R. 1999. An holistic approach to fish stock identification. Fish. Res. 43: 35-44. http://dx.doi.org/10.1016/S0165-7836(99)00065-X

Brookfield J.F.Y. 1996. A simple method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5: 453-455.

Brownstein M.J., Carpten J.D., Smith J.R. 1996. Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotech. 20(6):1004-6, 1008-10.

Carvalho G.R., Bembo D.G., Carone A., Giesbrecht G., Cingolani N., Pitcher T.J. 1994. Stock discrimination in relation to the assessment of Adriatic anchovy and sardine fisheries. Final Project Report to the Commission of the European Communities, EC XIV-1/MED/91001/A.

Chapuis M.P., Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24(3): 621-631. http://dx.doi.org/10.1093/molbev/msl191

Cingolani N., Santojanni A., Arneri E., Berlardinelli A., Colella S., Donato F., Giannetti G., Sinovčić G., Zorica B. 2004. Sardine (Sardina pilchardus, Walb.) stock assessment in the Adriatic Sea: 1975-2003. Paper presented at the GFCM-SAC working group on small pelagic species, Malaga, 6-7 May 2004. Food and Agriculture Organization project, Adriamed: scientific cooperation to support responsible fisheries in the Adriatic Sea. Adriamed Occasional Papers, 13, 9 pp.

Coates B.S., Sumerford D.V., Miller N.J., Kim K.S., Sappington T.W., Siegfried B.D. and Lewis L.C. 2009. Comparative Performance of Single Nucleotide Polymorphism and Microsatellite Markers for Population Genetic Analysis. J. Hered. 100(5): 556-564. http://dx.doi.org/10.1093/jhered/esp028

Dempster AP, Laird NM, Rubin DB. 1977. Maximum likelihood from incomplete data via the EM algorithm. J. R. Stat. Soc. B. 39: 1-38.

DeWoody J.A., Avise J.C. 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish Biol. 56: 461-473. http://dx.doi.org/10.1111/j.1095-8649.2000.tb00748.x

Durand J.D., Tine M., Panfili J., Thiaw O.T., Laë R. 2005. Impact of glaciations and geographic distance on the genetic structure of a tropical estuarine fish, Ethmalosa fimbriata (Clupeidae, S. Bowdich, 1825). Mol. Phyl. Evol. 36: 277-287. http://dx.doi.org/10.1016/j.ympev.2005.01.019

El Mousadik A., Petit R.J. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Gen. 92: 832-839. http://dx.doi.org/10.1007/BF00221895

Estoup A., Jarne P., Cornuet J.M. 2002. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol. Ecol. 11: 1591-1604. http://dx.doi.org/10.1046/j.1365-294X.2002.01576.x

Excoffier L., Laval G., Schneider S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.

Falush D., Stephens M., Pritchard J.K. 2003. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567-1587.

FAO 2005. Review of the state of world marine fishery resources. Marine Resources Service Fishery Resources Division. FAO Fisheries Department. FAO fisheries technical paper, 457.

Feyrer F., Hobbs J., Baerwald M., Sommer T., Yin Q., Clark K., May B., Bennett W. 2007. Otolith Microchemistry Provides Information Complementary to Microsatellite DNA for a Migratory Fish. Trans. Am. Fisher. Soc. 136: 469-476. http://dx.doi.org/10.1577/T06-044.1

FIGIS 2004. A world overview of species of interest to fisheries. Sardina pilchardus, Species Identification and Data Programme. FIGIS Species Fact Sheets. FAO-FIGIS.

Gonzalez E.G., Zardoya R. 2007a. Relative role of life-history traits and historical factors in shaping genetic population structure of sardines (Sardina pilchardus). BMR Evol. Biol. 7: 197. http://dx.doi.org/10.1186/1471-2148-7-197

Gonzalez E.G., Zardoya R. 2007b. Isolation and characterization of polymorphic microsatellites for the sardine, Sardina pilchardus (Clupleidae). Mol. Ecol. Notes 7: 519-521. http://dx.doi.org/10.1111/j.1471-8286.2006.01640.x

Goodman S.J. 1997. RstCalc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. Mol. Ecol. 6: 881-885. http://dx.doi.org/10.1111/j.1365-294X.1997.tb00143.x

Goudet J., Raymond M., DeMeeus T., Rousset F. 1996. Testing differentiation in diploid populations. Genetics 144: 1933-1940.

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

Grant W.S., Bowen B.W. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J. Hered. 89: 415-426. http://dx.doi.org/10.1093/jhered/89.5.415

Guo S., Thompson E. 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361-372. http://dx.doi.org/10.2307/2532296

Hauser L., Seeb J.E. 2008. Advances in molecular technology and their impact on fisheries genetics. Fish Fisher. 9: 473-486. http://dx.doi.org/10.1111/j.1467-2979.2008.00306.x

Hedrick P.W. 1999. Highly variable loci and their interpretation in evolution and conservation. Evolution 53: 313-318. http://dx.doi.org/10.2307/2640768

Hoarau G., Rijnsdorp A.D., Van der Veer H.W., Stam W.T., Olsen J.L. 2002. Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol. Ecol. 11: 1165-1176. http://dx.doi.org/10.1046/j.1365-294X.2002.01515.x

Kapuscinski A.R., Miller L.M. 2007. Genetic guidelines for fisheries management. University of Minnesota Sea Grant Program, pp. 1-114.

Kasapidis P., Silva A., Zampicini G., Magoulas A. 2012. Evidence for microsatellite hitchhiking selection in European sardine (Sardina pilchardus) and implications in inferring stock structure. Sci. Mar. 76(1): 123-132. http://dx.doi.org/10.3989/scimar.03366.29B

Kinsey S.T., Orsoy T., Bert T.M., Mahmoudi B. 1994. Population structure of the Spanish sardine Sardinella aurita: natural morphological variation in a genetically homogenous population. Mar. Biol. 118: 309-317. http://dx.doi.org/10.1007/BF00349798

Laurent V., Caneco B., Magoulas A., Planes S. 2007. Isolation by distance and selection effects on genetic structure of sardines Sardina pilchardus (Walbaum). J. Fish Biol. 71(a): 1-17.

Limborg M.T., Hanel R., Debes P.V., Ring A.K., André C., Tsigenopoulos C.S., Bekkevold D. 2012. Imprints from genetic drift and mutation imply relative divergence times across marine transition zones in a pan-European small pelagic fish (Sprattus sprattus). Heredity 109: 96-107. http://dx.doi.org/10.1038/hdy.2012.18

Maggio T., Lo Brutto S., Garoia F., Tinti F., Arculeo M. 2009. Microsatellite analysis on red mullet Mullus barbatus (Perciformes, Mullidae) reveals the isolation of the Adriatic Basin in the Mediterranean Sea. ICES J. Mar. Sci. 66(9): 1883-1891. http://dx.doi.org/10.1093/icesjms/fsp160

O'Connell M., Wright J.M. 1997. Microsatellite DNA in fishes. Rev. Fish Biol. Fisher. 7: 331-363. http://dx.doi.org/10.1023/A:1018443912945

O'Reilly P.T., Canino M.F., Bailey K.M., Bentzen P. 2004. Inverse 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. http://dx.doi.org/10.1111/j.1365-294X.2004.02214.x

Palumbi S.R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Ann. Rev. Ecol. Evol. Syst. 25: 547-572.

Pereyra R.T., Saillant E., Pruett C.L., Rexroad III C.E., Rocha-Olivares A., Gold J.R. 2004. Characterization of polymorphic microsatellites in the Pacific sardine Sardinops sagax sagax (Clupeidae). Mol. Ecol. Notes 4: 739-741.Pritchard J.K., Stephens http://dx.doi.org/10.1111/j.1471-8286.2004.00801.x

M., Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.

Rice W.R. 1989. Analysing tables of statistical tests. Evolution 43: 223-225. http://dx.doi.org/10.2307/2409177

Rousset F. 2008. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Res. 8: 103-106. http://dx.doi.org/10.1111/j.1471-8286.2007.01931.x

Ruggeri P., Splendiani A., Bonanomi S., Arneri E., Cingolani N., Santojanni A., Belardinelli A., Giovannotti M., Caputo V. 2012. Temporal genetic variation as revealed by a microsatellite analysis of European sardine (Sardina pilchardus) archived samples. Can. J. Fisher. Aquat. Sci. 69: 1698-1709. http://dx.doi.org/10.1139/f2012-092

Ryman N., Palm S. 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. Notes 6: 600-602. http://dx.doi.org/10.1111/j.1471-8286.2006.01378.x

Santojanni A., Cingolani N., Arneri E., Kirkwood G., Belardinelli A., Giannetti G., Colella S., Donato F., Barry C. 2005. Stock assessment of sardine (Sardina pilchardus, WALB.) in the Adriatic Sea, with an estimate of discards. Sci. Mar. 69(4): 603-617.

Slatkin M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787-792. http://dx.doi.org/10.1126/science.3576198

Slatkin M. 1993. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264-279. http://dx.doi.org/10.2307/2410134

Slatkin M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.

Spanakis E., Tsimenides N., Zouros E. 1989. Genetic differences between populations of sardine, Sardina pilchardus, and anchovy, Engraulis encrasicolus, in the Aegean and Ionian seas. J. Fish Biol. 35: 417-437. http://dx.doi.org/10.1111/j.1095-8649.1989.tb02993.x

Taggart J.B., Hynes R.A., Prodohol P.A., Ferguson A. 1992. A simplified protocol for routine total DNA isolation from salmonid fishes. J. Fish Biol. 40: 963-965. http://dx.doi.org/10.1111/j.1095-8649.1992.tb02641.x

Tinti F., Di Nunno C., Guarniero I., Talenti M., Tommasini S., Fabbri E., Piccinetti C. 2002. Mitochondrial DNA sequence variation suggests the lack of genetic heterogeneity in the Adriatic and Ionian stocks of Sardina pilchardus. Mar. Biotech. 4: 163-172. http://dx.doi.org/10.1007/s10126-002-0003-3

Van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535-538. http://dx.doi.org/10.1111/j.1471-8286.2004.00684.x

Waldman B., McKinnon J.S. 1993. Inbreeding and outbreeding in fishes, amphibians and reptiles. In: The natural history of inbreeding and outbreeding (ed. N.W. Thornbel). University of Chicago Press.

Waldman J.R. 2005. Definition of stocks: an evolving concept. In: Cadrin S.X., Friedland K.D., Waldman J.R. (eds.), Stock Identification Methods. Elsevier Academic Press, Burlington, MA, pp. 7-16. http://dx.doi.org/10.1016/B978-012154351-8/50003-4

Waples R.S., Gaggiotti O. 2006. What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol. Ecol. 15(6): 1419-1439. http://dx.doi.org/10.1111/j.1365-294X.2006.02890.x

Ward R.D. 2006. The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fisher. Res. 80: 9-18. http://dx.doi.org/10.1016/j.fishres.2006.03.009

Weir BS. 1996. Genetic data analysis II. Sunderland (MA): Sinauer Associates.

Weir B.S., Cockerham C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370. http://dx.doi.org/10.2307/2408641

Whitehead P.J.P. 1985. FAO species catalogue. Clupeid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings. Part 1. Chirocentridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis, 125(7).

Zardoya R., Castilho R., Grande C., Favre-Krey L., Caetano S., Marcato S., Krey G., Patarnello, T. 2004. Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Mol. Ecol. 13: 1785-1798. http://dx.doi.org/10.1111/j.1365-294X.2004.02198.x

Zarraonaindia I., Pardo M.A., Iriondo M., Manzano C., Estonba A. 2009. Microsatellite variability in European anchovy (Engraulis encrasicolus) calls for further investigation of its genetic structure and biogeography. ICES J. Mar. Sci., 66: 2176-2182. http://dx.doi.org/10.1093/icesjms/fsp187

Zouros E., Foltz D.W. 1984. Possible explanation of heterozygote deficiency in bivalve molluscs. Malacol. 25: 583-591.




Copyright (c) 2013 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es