Relative role of life-history traits and historical factors in shaping genetic population structure of sardines (Sardina pilchardus)

BackgroundMarine pelagic fishes exhibit rather complex patterns of genetic differentiation, which are the result of both historical processes and present day gene flow. Comparative multi-locus analyses based on both nuclear and mitochondrial genetic markers are probably the most efficient and informative approach to discerning the relative role of historical events and life-history traits in shaping genetic heterogeneity. The European sardine (Sardina pilchardus) is a small pelagic fish with a relatively high migratory capability that is expected to show low levels of genetic differentiation among populations. Previous genetic studies based on meristic and mitochondrial control region haplotype frequency data supported the existence of two sardine subspecies (S. p. pilchardus and S. p. sardina).ResultsWe investigated genetic structure of sardine among nine locations in the Atlantic Ocean and Mediterranean Sea using allelic size variation of eight specific microsatellite loci. Bayesian clustering and assignment tests, maximum likelihood estimates of migration rates, as well as classical genetic-variance-based methods (hierarchical AMOVA test and RSTpairwise comparisons) supported a single evolutionary unit for sardines. These analyses only detected weak but significant genetic differentiation, which followed an isolation-by-distance pattern according to Mantel test.ConclusionWe suggest that the discordant genetic structuring patterns inferred based on mitochondrial and microsatellite data might indicate that the two different classes of molecular markers may be reflecting different and complementary aspects of the evolutionary history of sardine. Mitochondrial data might be reflecting past isolation of sardine populations into two distinct groupings during Pleistocene whereas microsatellite data reveal the existence of present day gene flow among populations, and a pattern of isolation by distance.

[1]  B. Andreu Las branquispinas en la caracterización de las poblaciones de Sardina pilchardus (Walb) , 1969 .

[2]  I. Nakamura,et al.  Fao Species Catalogue , 1972 .

[3]  M. Nei,et al.  Estimation of fixation indices and gene diversities , 1983, Annals of human genetics.

[4]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[5]  P. Whitehead FAO Species Catalogue. Vol. 7. Clupeoid fishes of the world (suborder Clupeioidei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings , 1985 .

[6]  P. Whitehead Clupeoid fishes of the world (suborder Clupeoidei) : an annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies, and wolfherrings , 1985 .

[7]  J. Whitehead Clupeoid fishes of the world. FAO species catalogue Vol 7. An annoted and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolf herrings. Part 1 : Chirocentridae, Clupeidae and Pristigasteridae , 1985 .

[8]  M. Nei Molecular Evolutionary Genetics , 1987 .

[9]  R. Waples A MULTISPECIES APPROACH TO THE ANALYSIS OF GENE FLOW IN MARINE SHORE FISHES , 1987, Evolution; international journal of organic evolution.

[10]  Joaquín Tintoré,et al.  A study of an intense density front in the eastern Alboran Sea: the Almeria-Oran front , 1988 .

[11]  R. Serra,et al.  The Monotypic Sardines, Sardina and Sardinops: Their Taxonomy, Distribution, Stock Structure, and Zoogeography , 1989 .

[12]  E. Zouros,et al.  Genetic differences between populations of sardine, Sardina pilchardus, and anchovy, Engraulis encrasicolus, in the Aegean and Ionian seas , 1989 .

[13]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[14]  E. Thompson,et al.  Performing the exact test of Hardy-Weinberg proportion for multiple alleles. , 1992, Biometrics.

[15]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[16]  D. Skibinski,et al.  A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes , 1994 .

[17]  N. Freimer,et al.  Mutational processes of simple-sequence repeat loci in human populations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Tony J. Pitcher,et al.  Molecular Genetics in Fisheries , 1994, Springer Netherlands.

[19]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[20]  F. Bonhomme,et al.  GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. , 1996 .

[21]  J. Brookfield A simple new method for estimating null allele frequency from heterozygote deficiency , 1996, Molecular ecology.

[22]  L. Excoffier,et al.  A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. , 1996, Genetics.

[23]  J. Castro,et al.  Genetic variation in natural stocks of Sardina pilchardus (sardines) from the western Mediterranean Sea , 1997, Heredity.

[24]  B. Rannala,et al.  Detecting immigration by using multilocus genotypes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Goodman,et al.  RST Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance , 1997 .

[26]  Daniel E. Ruzzante,et al.  A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variance , 1998 .

[27]  J. Avise Conservation genetics in the marine realm , 1998 .

[28]  B. Bowen,et al.  Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation , 1998 .

[29]  J. Graves Molecular insights into the population structures of cosmopolitan marine fishes , 1998 .

[30]  B. Ely,et al.  Genetic evidence for inter-oceanic subdivision of bigeye tuna (Thunnus obesus) populations , 1998 .

[31]  E. D. Barton,et al.  Mesoscale distribution of fish larvae in relation to an upwelling filament off Northwest Africa , 1999 .

[32]  J. Felsenstein,et al.  Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. , 1999, Genetics.

[33]  D. A. Smith,et al.  The use of microsatellite variation to infer population structure and demographic history in a natural model system. , 1999, Genetics.

[34]  G. Luikart,et al.  Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data , 1999 .

[35]  J. Searle Phylogeography — The History and Formation of Species , 2000, Heredity.

[36]  D. Skagen,et al.  Phylogeography and population history of Atlantic mackerel (Scomber scombrus L.): a genealogical approach reveals genetic structuring among the eastern Atlantic stocks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[37]  DW J.A. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals , 2000 .

[38]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[39]  J. Graves,et al.  Reconciling patterns of inter‐ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans) , 2001, Molecular ecology.

[40]  J. Goudet FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995) , 2001 .

[41]  J. Salat,et al.  Comparative study of spatial distribution patterns of the early stages of anchovy and pilchard in the NW Mediterranean Sea , 2001 .

[42]  O. Hardy,et al.  spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels , 2002 .

[43]  Mitochondrial DNA Sequence Variation Suggests the Lack of Genetic Heterogeneity in the Adriatic and Ionian Stocks of Sardina pilchardus , 2002, Marine Biotechnology.

[44]  Myriam Heuertz,et al.  Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. , 2003, Genetics.

[45]  R. Sibly,et al.  Likelihood-based estimation of microsatellite mutation rates. , 2003, Genetics.

[46]  J. Graves,et al.  Stock structure of the world's istiophorid billfishes: a genetic perspective , 2003 .

[47]  N. Stenseth,et al.  Fine‐scaled geographical population structuring in a highly mobile marine species: the Atlantic cod , 2003, Molecular ecology.

[48]  S. Pálsson Isolation by distance, based on microsatellite data, tested with spatial autocorrelation (spaida) and assignment test (spassign) , 2004 .

[49]  G. Carvalho,et al.  Molecular genetics and the stock concept in fisheries , 1994, Reviews in Fish Biology and Fisheries.

[50]  K. Bailey,et al.  Inverse relationship between FST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure , 2004, Molecular ecology.

[51]  R. Zardoya,et al.  Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea , 2004, Molecular ecology.

[52]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[53]  J. Cornuet,et al.  Analytical bayesian approach for assigning individuals to populations. , 2004, The Journal of heredity.

[54]  C. Pla,et al.  Phylogeography of the Atlantic bonito (Sarda sarda) in the northern Mediterranean: the combined effects of historical vicariance, population expansion, secondary invasion, and isolation by distance. , 2004, Molecular phylogenetics and evolution.

[55]  R. Ward,et al.  Appraisal of molecular genetic techniques in fisheries , 1994, Reviews in Fish Biology and Fisheries.

[56]  R. Nielsen,et al.  Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species , 2004, Molecular ecology.

[57]  J. Graves,et al.  Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea , 2004, Molecular ecology.

[58]  J. Mejuto,et al.  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. , 2005, Molecular phylogenetics and evolution.

[59]  J. Durand,et al.  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 , 2005 .

[60]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[61]  E. Simmonds,et al.  North Sea herring population structure revealed by microsatellite analysis , 2005 .

[62]  M. B. Hamilton,et al.  Reconciling nuclear microsatellite and mitochondrial marker estimates of population structure: breeding population structure of Chesapeake Bay striped bass (Morone saxatilis) , 2005, Heredity.

[63]  Henrik Mosegaard,et al.  ENVIRONMENTAL CORRELATES OF POPULATION DIFFERENTIATION IN ATLANTIC HERRING , 2005, Evolution; international journal of organic evolution.

[64]  E. Beckwith,et al.  DROPOUT : a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework , 2005 .

[65]  E. Macpherson,et al.  Population structure within and between subspecies of the Mediterranean triplefin fish Tripterygion delaisi revealed by highly polymorphic microsatellite loci , 2006, Molecular ecology.

[66]  E. González,et al.  Genetic diversity and historical demography of Atlantic bigeye tuna (Thunnus obesus). , 2006, Molecular phylogenetics and evolution.

[67]  E. González,et al.  Signature of an early genetic bottleneck in a population of Moroccan sardines (Sardina pilchardus). , 2006, Molecular phylogenetics and evolution.

[68]  P. Lenfant,et al.  First approach for the identification of sardine populations Sardina pilchardus (Walbaum 1792) in the Moroccan Atlantic by allozymes , 2006 .

[69]  Johann R. E. Lutjeharms The Agulhas Current , 2006 .

[70]  D. Bekkevold,et al.  Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring , 2006, Proceedings of the Royal Society B: Biological Sciences.

[71]  J. Pella,et al.  The Gibbs and splitmerge sampler for population mixture analysis from genetic data with incomplete baselines , 2006 .

[72]  I. Koizumi,et al.  Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream‐dwelling Dolly Varden charr , 2006, Molecular ecology.

[73]  Costas Papaconstantinou,et al.  Spawning habitat and daily egg production of sardine (Sardina pilchardus) in the eastern Mediterranean , 2006 .

[74]  E. González,et al.  Isolation and characterization of polymorphic microsatellites for the sardine Sardina pilchardus (Clupeiformes: Clupeidae) , 2006 .

[75]  T. Patarnello,et al.  Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). , 2006, Molecular phylogenetics and evolution.

[76]  T. Atarhouch,et al.  Genetic population structure of sardine (Sardina pilchardus) off Morocco detected with intron polymorphism (EPIC-PCR) , 2007 .

[77]  G. Carvalho,et al.  Concordance of allozyme and microsatellite differentiation in a marine fish, but evidence of selection at a microsatellite locus , 2007, Molecular ecology.

[78]  J. Huelsenbeck,et al.  Inference of Population Structure Under a Dirichlet Process Model , 2007, Genetics.

[79]  G. Carvalho,et al.  Larsson LC, Laikre L, Palm S, Andre C, Carvalho GR, Ryman N. Concordance of allozyme and microsatellite differentiation in a marine fish, but evidence of selection at a microsatellite locus. Mol Ecol 16: 1135-1147 , 2007 .

[80]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.