Evidence for microsatellite hitchhiking selection in European sardine (Sardina pilchardus) and implications in inferring stock structure

Authors

  • Panagiotis Kasapidis Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics
  • Alexandra Silva Instituto de Investigação das Pescas e do Mar (INRB-IPIMAR)
  • Gianpaolo Zampicinini Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics - Dipartimento di Biologia Animale e dell’Uomo, Universita di Torino
  • Antonios Magoulas Hellenic Centre for Marine Research, Institute of Marine Biology and Genetics

DOI:

https://doi.org/10.3989/scimar.03366.29B

Keywords:

sardine, genetic structure, microsatellite DNA, selection, Atlantic, Mediterranean

Abstract


The genetic structure of the European sardine (Sardina pilchardus) was assessed throughout its geographic range using five microsatellite loci. One of the loci seemed to be under hitchhiking selection and exhibited a latitudinal cline along the eastern Atlantic, with abrupt change in allele frequencies from the Alboran Sea to the western Mediterranean and from the east Atlantic coast to the Azores and Madeira. This pattern was very similar to that previously described for the allozymic locus SOD* and these 2 loci could be linked. A Bayesian analysis of environmental factors with the genetic data indicated temperature as a potential selection factor. Selection pressure may be stronger at the southern limit of sardine distribution, because heterozygosity of the non-neutral locus was much lower there. The abrupt change in allele frequencies of the non-neutral locus in certain regions seem to be related more to strong barriers to gene flow, which were not evident for neutral loci, than to abrupt changes in selection pressure. These areas of discontinuity provide a guideline to define and delineate genetic stocks and are generally consistent with areas of phenotypic change in sardine, but they are not in concordance with the currently recognized morphological subspecies.

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References

Allendorf F.W., Phelps S.R. 1981. Use of allelic frequencies to describe population structure. Can. J. Fish Aquat. Sci. 38: 1507-1514. http://dx.doi.org/10.1139/f81-203

Andreu B. 1969. Las branquispinhas en la caracterizacion de las poblaciones de Sardina pilchardus (Walb.). Inv. Pesq. 33: 1-607.

Anonymous. 2006. Sardine dynamics and stock structure in the North-eastern Atlantic. Final Report. DGXIV Fisheries, European Commission, Brussels. Q5RS/2002/000818, available from yorgos@pimar.pt.

Atarhouch T., Rüber 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 PMid:16216537

Balding D.J., Nichols R.A. 1995. A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity. Genetica 96: 3-12. http://dx.doi.org/10.1007/BF01441146 PMid:7607457

Batargias C., Dermitzakis E., Magoulas A., Zouros E. 1999. Characterization of 6 polymorphic microsatellite markers in gilthead seabream, Sparus aurata. Mol. Ecol. 8: 897-899. PMid:10368971

Beaumont M.A., Nichols R.A. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B. Biol. Sci. 263: 1619-1626. http://dx.doi.org/10.1098/rspb.1996.0237

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 5171, Univ. Montpellier II, Montpellier (France).

Carvalho G., Hauser L. 1998. Advances in the molecular analysis of fish population structure. Ital. J. Zool. 65(Suppl): 21-33 http://dx.doi.org/10.1080/11250009809386791

Chlaida M., Kifani S., Lenfant P., Ouragh L. 2006. First approach for the identification of sardine populations Sardina pilchardus (Walbaum 1792) in the Moroccan Atlantic by allozymes. Mar. Biol. 149: 169-175. http://dx.doi.org/10.1007/s00227-005-0185-0

Chlaida M., Laurent V., Kifani S., Benazzou T., Jaziri H., Planes S. 2009. Evidence of a genetic cline for Sardina pilchardus along the Northwest African coast. ICES J. Mar. Sci. 66: 264-271. http://dx.doi.org/10.1093/icesjms/fsn206

Conover D.O., Clarke L.M., Munch S.B., Wagner G.N. 2006. Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J. Fish Biol. 69 (Suppl C): 21-47. http://dx.doi.org/10.1111/j.1095-8649.2006.01274.x

Coombs S.H., Smyth T.J., Conway D.V.P., Halliday N.C., Bernal M., Stratoudakis Y., Alvarez P. 2006. Spawning season and temperature relationships for sardine (Sardina pilchardus) in the eastern North Atlantic. J. Mar. Biol. Assoc. UK 86: 1245-1252. http://dx.doi.org/10.1017/S0025315406014251

Dupanloup I., Schneider S., Excoffier L. 2002. A simulated annealing approach to define the genetic structure of populations. Mol. Ecol. 11: 2571-81. http://dx.doi.org/10.1046/j.1365-294X.2002.01650.x PMid:12453240

Excoffier L., Smouse P., Quattro J. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491. PMid:1644282    PMCid:1205020

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

Excoffier L., Hofer T., Foll M. 2009. Detecting loci under selection in a hierarchically structured population. Heredity 103: 285-298. http://dx.doi.org/10.1038/hdy.2009.74 PMid:19623208

FAO 2008. Report of the FAO Working Group on the Assessment of Small Pelagic Fish off Northwest Africa. Saly, Senegal, 6-15 May 2008. FAO Fish Rep. No. 882.

FAO 2009. Report of the SCSA working group on stock assessment of small pelagic species. GFCM: SAC12/2010/Inf.14.

Foll M., Gaggiotti O.E. 2006. Identifying the environmental factors that determine the genetic structure of populations. Genetics 174: 875-891. http://dx.doi.org/10.1534/genetics.106.059451 PMid:16951078    PMCid:1602080

Foll M., Gaggiotti O.E. 2008. A genome scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics 180: 977-993. http://dx.doi.org/10.1534/genetics.108.092221 PMid:18780740    PMCid:2567396

Ganias K., Somarakis S., Machias A., Theodorou A. 2003. Evaluation of spawning frequency in a Mediterranean sardine population. Mar. Biol. 142: 1169-1179.

Ganias K., Somarakis S., Machias A., Theodorou A. 2004. Pattern of oocyte development and batch fecundity in the Mediterranean sardine. Fish. Res. 67: 13-23. http://dx.doi.org/10.1016/j.fishres.2003.08.008

Gaggiotti O.E., Bekkevold D., Jorgensen H.B.H., Foll M., Carvalho G.R., Andre C., Ruzzante D.E. 2009. Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63: 2939-2951. http://dx.doi.org/10.1111/j.1558-5646.2009.00779.x PMid:19624724

Gauldie R.W. 1988. Tagging and genetically isolated stocks of fish: a test of one stock hypothesis and the development of another. J. Appl. Ichth. 4: 168-173. http://dx.doi.org/10.1111/j.1439-0426.1988.tb00557.x

Goudet J. 1995. Fstat version 1.2: a computer program to calculate Fstatistics. J. Heredity 86: 485-486.

GFCM 2006. Report of the eighth session of the sub-committee on stock assessment (SCSA). GFCM:SAC9/2006/Inf.8. ftp://ftp.fao.org _/DOCUMENT/gfcm/sac9/inf8e.pdf

Gonzalez E.G., Zardoya R. 2007a. Relative role of life-history traits and historical factors in shaping genetic population structure of sardines (Sardina pilchardus). BMC Evol. Biol. 7: 197- 209. http://dx.doi.org/10.1186/1471-2148-7-197 PMid:17953768    PMCid:2204010

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

Guinand B., Lemaire C., Bohnomme F. 2004. How to detect polymorphisms undergoing selection in marine fishes? A review of methods and case studies, including flatfishes. J. Sea Res. 51: 167-182. http://dx.doi.org/10.1016/j.seares.2003.10.002

Hemmer-Hansen J., Nielsen E.E., Frydenberg J., Loeschcke V. 2007. Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity 99: 592-600. http://dx.doi.org/10.1038/sj.hdy.6801055 PMid:17848973

ICES 2006. Report of the Working Group on the Assessment of Mackerel, Horse Mackerel, Sardine, and Anchovy. ICES Document CM 2006/ACFM: 36.

ICES 2009. Report of the Working Group on Anchovy and Sardine. ICES Document CM 2009/ACOM:13.

Jensen J.L., Bohonak A.J., Kelley S.T. 2005. Isolation by distance, web service. BMC Genetics 6: 13. http://dx.doi.org/10.1186/1471-2156-6-13 PMid:15760479    PMCid:1079815

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: 1-17. http://dx.doi.org/10.1111/j.1095-8649.2007.01450.x

Mäkinen H.S., Cano J.M., Merilä J. 2008. Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol. Ecol. 17: 3565-3582. http://dx.doi.org/10.1111/j.1365-294X.2008.03714.x PMid:18312551

Maynard Smith J., Haigh J. 1974. The hitch–hiking effect of a favourable gene. Genet. Res. 23: 23-35. http://dx.doi.org/10.1017/S0016672300014634

Miller S.A., Dykes D.D., Polesky H.F. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16: 1215. http://dx.doi.org/10.1093/nar/16.3.1215 PMid:3344216    PMCid:334765

Moen T., Hayes B., Nilsen F., Delghandi M., Fjalestad K., Fevolden S.E., Berg P., Lien S. 2008. Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genetics 9: 18. http://dx.doi.org/10.1186/1471-2156-9-18 PMid:18302786    PMCid:2288615

Nielsen E.E., Hemmer-Hansen J., Larsen P.F., Bekkevold D. 2009. Population genomics of marine fishes: identifying adaptive variation in space and time. Mol. Ecol. 18: 3128-3150. http://dx.doi.org/10.1111/j.1365-294X.2009.04272.x PMid:19627488

Nosil P., Funk D.J., Ortiz-Barrientos D. 2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18: 375-402. http://dx.doi.org/10.1111/j.1365-294X.2008.03946.x PMid:19143936

Ovenden J.R. 1990. Mitochondrial DNA and marine stock assessment: a review. Aust. J. Mar. Freshwater Res. 41: 835-853. http://dx.doi.org/10.1071/MF9900835

Patarnello T., Volckaert A.M.J., Castilho R. 2007. Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Mol. Ecol. 16: 4426-4444. http://dx.doi.org/10.1111/j.1365-294X.2007.03477.x PMid:17908222

Parrish R.H., Serra R., Grant W.S. 1989. The monotypic Sardines, Sardina and Sardinops: their taxonomy, distribution, stock structure, and zoogeography. Can. J. Fish. Aquat. Sci. 46: 2019-2036. http://dx.doi.org/10.1139/f89-251

Pogson G.H. 2001. Nucleotide polymorphism and natural selection at the pantophysin (Pan I) locus in the Atlantic cod, Gadus morhua (L.). Genetics 157: 317-330. PMid:11139512    PMCid:1461473

Raymond M., Rousset F. 1995. GENEPOP (version1.2): population genetics software for exact tests and ecumenism. J. Heredity 86: 248-249.

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

Schulte P.M., Glemet H.C., Fiebig A.A., Powers D.A. 2000. Adaptive variation in lactate dehydrogenase-B gene expression: role of a stress-responsive regulatory element. Proc. Natl. Acad. Sci. USA 97: 6597-6602. http://dx.doi.org/10.1073/pnas.97.12.6597

Simonsen K.L., Churchill G.A., Aquadro C.F. 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413-429. PMid:8536987    PMCid:1206737

Silva A. 2003. Morphometric variation among sardine (Sardina pilchardus) populations from the northeastern Atlantic and the western Mediterranean. ICES J. Mar. Sci. 60: 1352-1360. http://dx.doi.org/10.1016/S1054-3139(03)00141-3

Silva A., Santos M.B., Caneco B., Pestana G., Porteiro C., Carrera P., Stratoudakis Y. 2006. Temporal and geographic variability of sardine maturity at length in the north-eastern Atlantic and the western Mediterranean. ICES J. Mar. Sci. 63: 663-676. http://dx.doi.org/10.1016/j.icesjms.2006.01.005

Silva A., Carrera P., Massé J., Uriarte A.D., Santos M.B., Oliveira P.B., Soares E., Porteiro C., Stratoudakis Y. 2008. Geographic variability of sardine growth across the northeastern Atlantic and the Mediterranean Sea. Fish. Res. 90: 56-69. http://dx.doi.org/10.1016/j.fishres.2007.09.011

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

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 PMid:14961276

Tsigenopoulos C.S., Hellemans B., Chistiakov D.A., Libertini A., Kotoulas G., Volckaert F. 2003. Eleven new microsatellites of the sea bass (Dicentrarchus labrax L.). Mol. Ecol. Notes 3: 352-354. http://dx.doi.org/10.1046/j.1471-8286.2003.00447.x

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

Waples R.S. 1998. Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J. Heredity 89: 438-450. http://dx.doi.org/10.1093/jhered/89.5.438

Ward R.D. 2000. Genetics in fisheries management. Hydrobiologia 420: 191-201. http://dx.doi.org/10.1023/A:1003928327503

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

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Published

2012-03-30

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1.
Kasapidis P, Silva A, Zampicinini G, Magoulas A. Evidence for microsatellite hitchhiking selection in European sardine (Sardina pilchardus) and implications in inferring stock structure. Sci. mar. [Internet]. 2012Mar.30 [cited 2024Mar.28];76(1):123-32. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1316

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