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Marine Biology

, Volume 155, Issue 3, pp 325–336 | Cite as

Phylogeography of the Southwestern Atlantic menhaden genus Brevoortia (Clupeidae, Alosinae)

  • Graciela García
  • Julia Vergara
  • Verónica Gutiérrez
Original Paper

Abstract

Among pelagic fish, the Southwestern Atlantic menhaden genus Brevoortia (Clupeidae, Alosinae) constitutes an important species model to investigate the patterns of genetic differentiation. It is abundant in the Río de la Plata estuary and in the Atlantic coastal lagoons system from Uruguay and Southern Brazil. To access in the taxa discrimination and population structure in Brevoortia we perform a phylogeographic approach based on mitochondrial cytochrome b (cyt-b) sequences including 240 individuals from 16 collecting sites. Among the 720 bp cyt-b sequenced, 199 correspond to variables and 88 to phylogenetically informative sites. High values of haplotype diversity (h = 1.000) and nucleotide diversity (π = 0.061), as well as an average of 0.084 polymorphic segregating sites and 46 different haplotypes were found. Maximum likelihood analysis based on the GTR + I + G model and Bayesian inference strongly support the idea that B. aurea is the only species of the genus inhabiting the Southwestern Atlantic region. Our analyses revealed a complex population pattern characterized by the existence of long-term highly structured genetic assemblages of mixed stocks. Each monophyletic entity included individuals from different collecting sites, different age groups and collected in different years. Our data also suggest that the recruitment of unrelated mtDNA haplotypes carried out by individuals within schools could be occurring in the same nursery areas revealing the existence of many different maternal lineages. A scenario where different simultaneously and successively mixed mtDNA lineages remain historically connected through basal haplotypes among different clades could explains more accurately the complex and ordered metapopulation dynamic found in this pelagic fish.

Keywords

Coastal Lagoon Pelagic Fish Estuarine Environment Nursery Area Purse Seine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank the following people: J. M. Díaz de Astarloa for kindly donated individuals of B. aurea from Mar Chiquita lagoon (Argentina), and particularly to the fishermans Freddy Seija, German, Richard and Teresa Acosta from Rocha and Castillos lagoons (Uruguay) respectively, for kindly provided specimens of this species. We are grateful to G. Martínez, S. Retta to kindly supplied additional menhaden samples from 1999 to 2000 as well as to provided a morphological identification of adults and juveniles specimens in research collaboration with M. Azpelicueta. This manuscript is enriched by the comments of three anonymous reviewers. This research received financial support from the Project PDT 07-12-DINACYT-BID. The authors are also grateful to the Japanese government for the equipment donation.

References

  1. Acha EM, Macchi GJ (2000) Spawning of Brazilian menhaden, Brevoortia aurea, in the Río de la Plata estuary of Argentina and Uruguay. Fish Bull 98(2):227–235Google Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. doi: https://doi.org/10.1109/TAC.1974.1100705 CrossRefGoogle Scholar
  3. Anderson JD (2007) Systematics of the North American menhadens: molecular evolutionary reconstructions in the genus Brevoortia (Clupeiformes: Clupeidae). Fish Bull (Wash DC) 205:368–378Google Scholar
  4. Beheregaray LB, Sunnucks P (2001) Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Mol Ecol 10:2849–2866. doi: https://doi.org/10.1046/j.1365-294X.2001.t01-1-01406.x CrossRefGoogle Scholar
  5. Bilton DT, Paula J, Bishop JD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952. doi: https://doi.org/10.1006/ecss.2002.1037 CrossRefGoogle Scholar
  6. Blaber SJM, Blaber TG (1980) Factors affecting the distribution of juvenile estuarine and inshore fish. J Fish Biol 17:143–162. doi: https://doi.org/10.1111/j.1095-8649.1980.tb02749.x CrossRefGoogle Scholar
  7. Boschi EE (1988) El ecosistema estuarial del Río de la Plata (Argentina y Uruguay). Anales del Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autonoma de Mexico 15:159–182Google Scholar
  8. Bowen BW, Avise JC (1990) Genetic structure of Atlantic and Gulf of Mexico populations of sea bass, menhaden, and sturgeon: influence of zoogeographic factors and life-history patterns. Mar Biol 107:371–381. doi: https://doi.org/10.1007/BF01313418 CrossRefGoogle Scholar
  9. Cousseau MB (1985) Los peces del Río de la Plata y su Frente Marítimo. In: Yánez-Arancibia A (ed) Fish community ecology in estuaries and coastal lagoons: towards an ecosystem integration. UNAM Press, México, pp 515–534Google Scholar
  10. Cousseau MB, Díaz de Astarloa JM (1993) El género Brevoortia en la costa Atlántica sudamericana. Frente Maritimo 14:49–57Google Scholar
  11. Durand JD, Tine M, Panfili J, Thiaw OT, 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 Phylogenet Evol 36:277–287. doi: https://doi.org/10.1016/j.ympev.2005.01.019 CrossRefGoogle Scholar
  12. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  13. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  14. Grant WS (1985) Biochemical genetic stock structure of the South African anchovy, Engraulis capensis Gilchrist. J Fish Biol 27:23–29. doi: https://doi.org/10.1111/j.1095-8649.1985.tb04006.x CrossRefGoogle Scholar
  15. Grant WS, Bowen BW (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. doi: https://doi.org/10.1093/jhered/89.5.415 CrossRefGoogle Scholar
  16. Graves JE (1998) Molecular insights into the population structures of cosmopolitan marine fishes. J Hered 89:427–437. doi: https://doi.org/10.1093/jhered/89.5.427 CrossRefGoogle Scholar
  17. Harrison RG (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol Evol 4:6–11. doi: https://doi.org/10.1016/0169-5347(89)90006-2 CrossRefGoogle Scholar
  18. Hauser L, Carvalho GR, Pitcher TJ (1998) Genetic structure in the Lake Tanganyika sardine Limnothrissa miodon. J Fish Biol 53:413–429CrossRefGoogle Scholar
  19. Hildebrand SF (1948) A review of the American menhaden, genus Brevoortia with a description of a new species. Smithson Misc Collect 107:1–38Google Scholar
  20. Huelsenbeck JP (2001) MrBayes: Bayesian inference of phylogeny. Distributed by the author, Department of Biology, University of Rochester, New YorkGoogle Scholar
  21. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688. doi: https://doi.org/10.1080/10635150290102366 CrossRefGoogle Scholar
  22. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi: https://doi.org/10.1007/BF01731581 CrossRefGoogle Scholar
  23. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedPubMedCentralGoogle Scholar
  24. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA 2. Version 2.0. Molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245. doi: https://doi.org/10.1093/bioinformatics/17.12.1244 CrossRefGoogle Scholar
  25. Lasta CA, Ciechomski JD (1988) Primeros resultados de los estudios sobre la distribución de huevos y larvas de peces en Bahía Samborombón en relación a temperatura y salinidad. Publicacion de la Comision Tecnica Mixta del Frente Maritimo 4:133–141Google Scholar
  26. Liedloff A (1999) Mantel nonparametric test calculator for windows. Version 2.00. Distributed by the author, School of Natural Resource Sciences, Queensland University of Technology, BrisbaneGoogle Scholar
  27. Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220Google Scholar
  28. Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43PubMedGoogle Scholar
  29. Menezes NA, Buckup PA, de Figueredo JL, de Moura RL (2003) Catálogo das espécies de peixes marinhos do Brasil. Museu de Zoologia de Universidade de Sao Paulo, Sao PauloGoogle Scholar
  30. Menni RC, Ringuelet RA, Aramburu RH (1984) Peces marinos de la Argentina y Uruguay (Reseña histórica, clave de familia, géneros y especies, catálogo crítico). Hemisferio Sur S.A., Buenos Aires, 359 pGoogle Scholar
  31. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  32. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. doi: https://doi.org/10.1146/annurev.es.25.110194.002555 CrossRefGoogle Scholar
  33. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, HonoluluGoogle Scholar
  34. Posada D, Crandall A (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: https://doi.org/10.1093/bioinformatics/14.9.817 CrossRefGoogle Scholar
  35. Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311. doi: https://doi.org/10.1007/BF02338839 CrossRefGoogle Scholar
  36. Reintjes JW (1969) Synopsis of biological data on the Atlantic menhaden Brevoortia tyrannus. U.S. Fish Wildl Serv Circ 320:1–30Google Scholar
  37. Rodríguez F, Oliver JL, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501. doi: https://doi.org/10.1016/S0022-5193(05)80104-3 CrossRefGoogle Scholar
  38. Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi: https://doi.org/10.1093/bioinformatics/btg359 CrossRefGoogle Scholar
  39. Ruzzante DE, Mariani S, Bekkevold D, André C, Mosegaard H, Clausen LAW et al (2006) Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring. Proc R Soc Lond B Biol Sci 273:1459–1464. doi: https://doi.org/10.1098/rspb.2005.3463 CrossRefGoogle Scholar
  40. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. University of Geneva, GenevaGoogle Scholar
  41. Segura V, Díaz de Astarloa J (2004) Análisis osteológico de la saraca Brevoortia aurea (Spix) (Actinopterygii: Clupeidae) en el Atlántico suroccidental. Revista de Biologia Marina y Oceanografia 39:37–52Google Scholar
  42. Sinclair M, Iles TD (1989) Population regulation and speciation in the oceans. J Cons Int Explor Mer 45:165–175CrossRefGoogle Scholar
  43. Slatkin M (1991) Inbreeding coefficients and coalescence times. Genet Res 58:167–175CrossRefGoogle Scholar
  44. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  45. Sprechman P (1978) The paleoecology and paleogeography of the Uruguayan coastal area during the Neogene and Quaternary. Zitteliana 4:3–72Google Scholar
  46. Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b8. Sinauer Associates, SunderlandGoogle Scholar
  47. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  48. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi: https://doi.org/10.1093/nar/25.24.4876 CrossRefGoogle Scholar
  49. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450. doi: https://doi.org/10.1093/jhered/89.5.438 CrossRefGoogle Scholar
  50. Ward RD (1995) Population genetics of tunas. J Fish Biol 47:259–280. doi: https://doi.org/10.1111/j.1095-8649.1995.tb06060.x CrossRefGoogle Scholar
  51. Watterson GA (1984) Allele frequencies after a bottleneck. Theor Popul Biol 26:387–407. doi: https://doi.org/10.1016/0040-5809(84)90042-X CrossRefGoogle Scholar
  52. Whitehead PJP (1985) FAO species catalogue. Clupeoid fishes of the world (suborder Clupeoidei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, anchovies and wolf-herrings. Part 1—Chirocentridae, Clupeidae and Pristigasteridae. FAO Fisheries Synopsis no. 125, vol 7. FAO, Rome, pp 1–303Google Scholar
  53. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Graciela García
    • 1
  • Julia Vergara
    • 1
  • Verónica Gutiérrez
    • 1
  1. 1.Sección Genética Evolutiva, Facultad de CienciasUdelaRMontevideoUruguay

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