Skip to main content

Genetic characterization of Argentinean Artemia species with different fatty acid profiles

Abstract

The Anostracan genus Artemia is composed by several sibling species reproductively isolated, but identical or very similar in outward appearance. The genus shows also an underlying striking variability from the biochemical point of view, regarding especially the fatty acid profile of the cysts and nauplii. In Argentina, Artemia is represented by two bisexual species: A. franciscana and A. persimilis. Former studies have shown that A. franciscana is present in northern of 36º and that A. persimilis is constrained southwards of 37° S. In general, there is good agreement between morphological and cytogenetic comparisons of Argentinean populations with respect to species discrimination. However, new Argentinean Artemia populations are being analyzed morphologically and it becomes necessary to further investigate if the genetic adscription of these populations is congruent with the results obtained from the current morphological analyses. Restriction fragment length polymorphism (RFLP) analysis of a fragment of the 16S rRNA mitochondrial gene was used to investigate the genetic diversity and population structure of 10 new Artemia populations from Argentina. The mitochondrial DNA (mtDNA) results showed a similar pattern to that of previous cytogenetic and morphological analyses with the two Argentinean species appearing as highly divergent. The presence of A. persimilis in southern Argentina and the southernmost Chilean population was confirmed unveiling a novel picture of species distribution in the country. A. franciscana showed a unique haplotype. Populations of A. persimilis appeared highly structured, although their clustering did not follow a clear geographic pattern. The different Argentinean Artemia populations analyzed were characterized by high variability in their fatty acids, showing both marine- and freshwater-type profiles. For the first time, the investigation of the relatedness between the fatty acid composition in Artemia and genetic markers was attempted. The study aimed at the putative association of molecular markers with marine versus freshwater-type populations. A lack of correlation between RFLP patterns at mtDNA and the fatty acid (FA) profiles was found in the A. persimilis populations which was discussed from the point of view of two main genetic hypotheses and/or phenotypic plasticity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abreu-Grobois, F. A., 1987. A review of the genetics of Artemia. In Sorgeloos, P., D. A. Bengtson, W. Decleir & E. Jaspers (eds), Artemia Research and its Applications. Universa Press, Belgium: 61–99.

    Google Scholar 

  2. Amat, F., F. Hontoria, J. C. Navarro, R. G. Cohen & S. Rodríguez, 1994. Aproximación preliminar a la distribución del género Artemia (especie A persimilis) en Argentina Provincias de Buenos Aires y La Pampa. Actas VIII Congreso Latinoamericano de Acuicultura, Colciencias, Bogota, Colombia: 73–82.

  3. Amat, F., R. G. Cohen, F. Hontoria & J. C. Navarro, 2004. Further evidence and characterization of Artemia franciscana (Kellogg, 1906) populations in Argentina. Journal Biogeography 31: 1735–1749.

    Article  Google Scholar 

  4. Amat, F., F. Hontoria, O. Ruiz, A. J. Green, M. I. Sánchez, J. Figueroa & F. Hortas, 2005. The American brine shrimp as an exotic invasive species in the western Mediterranean. Biological Invasions 7: 37–47.

    Article  Google Scholar 

  5. Badaracco, G., L. Baratelli, E. Ginelli, R. Meneveri, P. Plevani, P. Valsasnini & C. Barigozzi, 1987. Variations in repetitive DNA and heterochromatin in the genus Artemia. Chromosoma 95: 71–75.

    Article  Google Scholar 

  6. Badaracco, G., M. Bellorini & N. Landsberger, 1995. Phylogenetic study of bisexual Artemia using random amplified polymorphic DNA. Journal of Molecular Evolution 41: 150–154.

    PubMed  Article  CAS  Google Scholar 

  7. Baratelli, L. & C. Barigozzi, 1990. Chromosome length: A differentiation parameter in the genus Artemia. Rendiconti Accademia Nazionale dei Lincei, Classe di Scienze Fisiche, Matematiche e Naturali, Serie 9: 459–464.

    Google Scholar 

  8. Baxevanis, A. D. & T. J. Abatzopoulos, 2004. The phenotypic response of ME2 (M Embolon, Greece) Artemia clone to salinity and temperature. Journal Biological Research 1: 107–114.

    Google Scholar 

  9. Baxevanis, A. D., G. V. Triantaphyllidis, I. Kappas, A. Triantafyllidis, C. D. Triantaphyllidis & T. J. Abatzopoulos, 2005. Evolutionary assessment of Artemia tibetiana (Crustacea, Anostraca) based on morphometry and 16S rRNA RFLP analysis. Journal of Zoological Systematics and Evolutionary Research 43: 189–198.

    Article  Google Scholar 

  10. Baxevanis, A. D., I. Kappas & T. J. Abatzopoulos, 2006. Molecular phylogenetics and asexuality in the brine shrimp Artemia. Molecular Phylogenetic Evolution 40: 724–738.

    Article  CAS  Google Scholar 

  11. Cohen, R. G., F. Amat, F. Hontoria & J. C. Navarro, 1999. Preliminary characterization of some Argentinean Artemia populations from La Pampa and Buenos Aires provinces. International Journal of Salt Lake Research 8: 329–340.

    Google Scholar 

  12. Colihueque, N. & G. Gajardo, 1996. Chromosomal analysis in Artemia populations from South America. Cytobios 88: 141–148.

    Google Scholar 

  13. Dragó, E. & R. Quirós, 1996. The hydrochemistry of the inland waters of Argentina: a review. International Journal of Salt Lake Research 4: 315–325.

    Article  Google Scholar 

  14. Estoup, A., C. R. Largiader, E. Perrot & D. Chourrout, 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Molecular Marine Biology and Biotechnology 5: 295–298.

    CAS  Google Scholar 

  15. Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    PubMed  CAS  Google Scholar 

  16. Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin version 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.

    CAS  PubMed  Google Scholar 

  17. Felsenstein, J., 2004. PHYLIP (Phylogeny Inference Package) Version 36c Distributed by the author Department of Genome Sciences. University of Washington, Seattle.

    Google Scholar 

  18. Gajardo, G., M. Da Conceicao, L. Weber & J. A. Beardmore, 1995. Genetic variability and interpopulational differentiation of Artemia strains from South America. Hydrobiologia 302: 21–29.

    Article  Google Scholar 

  19. Gajardo, G., N. Colihueque, M. Parraguez & P. Sorgeloos, 1998. International Study on Artemia LVIII. Morphologic differentiation and reproductive isolation of Artemia populations from South America. International Journal of Salt Lake Research 7: 133–151.

    Google Scholar 

  20. Gajardo, G., C. Mercado, J. A. Beardmore & P. Sorgeloos, 1999. International Study on Artemia LX. Allozyme data suggest that a new Artemia population in southern Chile (50°29′ S; 73°45′ W) is A persimilis. Hydrobiologia 405: 117–123.

    Article  Google Scholar 

  21. Gajardo, G., J. A. Beardmore & P. Sorgeloos, 2001. International Study on Artemia LXII Genomic relationships between Artemia franciscana and A persimilis, inferred from chromocentre numbers. Heredity 87: 172–177.

    PubMed  Article  CAS  Google Scholar 

  22. Gajardo, G., T. J. Abatzopoulos, I. Kappas & J. A. Beardmore, 2002. Evolution and speciation. In Abatzopoulos, T. J., J. A. Beardmore, J. S. Clegg & P. Sorgeloos (eds), Artemia: Basic and Applied Biology. Kluwer Academic Publishers, Dordrecht, The Netherlands: 225–250.

    Google Scholar 

  23. Gajardo, G., J. Crespo, A. Triantaphyllidis, A. Tzika, A. D. Baxevanis, I. Kappas & T. J. Abatzopoulos, 2004. Species identification of Chilean Artemia populations based on mitochondrial DNA RFLP analysis. Journal of Biogeography 31: 547–555.

    Article  Google Scholar 

  24. Green, A. J., M. I. Sánchez, F. Amat, J. Figuerola, F. Hontoria, O. Ruiz & F. Hortas, 2005. Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnology and Oceanography 50: 737–742.

    Article  Google Scholar 

  25. Hontoria, F. & F. Amat, 1992. Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origin: American populations. Journal of Plankton Research 14: 1461–1471.

    Article  Google Scholar 

  26. Lavens, P. & P. Sorgeloos, 2000. The history, present status and prospects of the availability of Artemia cysts for aquaculture. Aquaculture 181: 397–403.

    Article  Google Scholar 

  27. Lavens, P., P. Léger & P. Sorgeloos, 1989. Manipulation of the fatty acid profile in Artemia offspring produced in intensive culture systems. In De Paw, N., E. Jaspers, H. Ackefors & N. Wilkins (eds), Aquaculture: Biotechnology in Progress. European Aquaculture Society, Bredene: 731–739.

    Google Scholar 

  28. Léger, P., D. A. Bengtson, P. M. Simpson & P. Sorgeloos, 1986. The use and nutritional value of Artemia as a food source. Oceanography and Marine Biology: An Annual Review 24: 521–623.

    Google Scholar 

  29. Mantel, N., 1967. Detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.

    PubMed  CAS  Google Scholar 

  30. Medina, G. R., J. Goenaga, F. Hontoria, G. Cohen & F. Amat, 2007. Effects of temperature and salinity on prereproductive life span and reproductive traits of two species of Artemia (Branchiopoda, Anostraca) from Argentina: Artemia franciscana and Artemia persimilis. Hydrobiologia 579: 41–53.

    Article  Google Scholar 

  31. McElroy, D., P. Moran, E. Bermingham & I. Kornfield, 1992. REAP - An Integrated environment for the manipulation and phylogenetic analysis of restriction data. Journal of Heredity 83: 157–158.

    PubMed  CAS  Google Scholar 

  32. Navarro, J. C., 1990. Caracterización de las cepas españolas de Artemia desde el punto de vista de su valor nutritivo y de sus fenotipos electroforéticos Implicaciones prácticas en Acuicultura. Universidad de Valencia, España, MS Thesis, 350 pp.

  33. Navarro, J. C. & F. Amat, 1992. Effect of algal diets on the fatty acid composition of brine shrimp, Artemia sp cysts. Aquaculture 101: 223–227.

    Article  CAS  Google Scholar 

  34. Navarro, J. C., F. Amat & J. R. Sargent, 1993. The lipids of the cysts of freshwater-and marine-type Artemia. Aquaculture 109: 327–336.

    Article  CAS  Google Scholar 

  35. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York: 512 pp

    Google Scholar 

  36. Nei, M. & J. C. Miller, 1990. A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics 125: 873–879.

    PubMed  CAS  Google Scholar 

  37. Nei, M. & F. Tajima, 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.

    PubMed  CAS  Google Scholar 

  38. Palumbi, S. R., 1996. Nucleic acids II: the polymerase chain reaction. In Hillis, D. M., C. Moritz & B. K. Mable (eds), Molecular Systematics. Sinauer Associates, Sunderland: 205–247.

    Google Scholar 

  39. Papeschi, A. G., R. G. Cohen, G. Pastorino & F. Amat, 2000. Cytogenetic proof that the brine shrimp Artemia franciscana (Crustacea, Branchiopoda) is found in Argentina. Hereditas 133: 159–166.

    PubMed  Article  CAS  Google Scholar 

  40. Rodríguez-Gil, S., A. G. Papeschi & R. G. Cohen, 1998. Mitotic and meiotic chromosomes of Artemia (Branchiopoda) from populations of La Pampa province, Argentina. Journal of Crustacean Biology 18: 36–41.

    Article  Google Scholar 

  41. Roff, D. A. & P. Bentzen, 1989. The statistical analysis of mitochondrial DNA polymorphisms: χ2 and the problem of small samples. Molecular Biology and Evolution 6: 539–545.

    PubMed  CAS  Google Scholar 

  42. Ruiz, O., G. R. Medina, G. Cohen, F. Amat & J. C. Navarro, 2007. Diversity of the fatty acid composition of Artemia sp cysts from Argentinean populations. Marine Ecology Progress Series 335: 155–165.

    Article  CAS  Google Scholar 

  43. Sun, Y., W. Q. Song, Y. Zhong, R. S. Zhang, T. J. Abatzopoulos & R. Y. Chen, 1999. Diversity and genetic differentation in Artemia species and populations detected by AFLP markers. International Journal of Salt Lake Research 8: 341–350.

    Google Scholar 

  44. Tizol-Correa, R., L. Carreon-Palau, B. O. Arredondo-Vega, G. Murugan, L. Torrentera, T. D. Maldonado-Montiel & A. M. Maeda-Martinez, 2006. Fatty acid composition of Artemia (Branchiopoda: Anostraca) cysts from tropical salterns of southern Mexico and Cuba. Journal of Crustacean Biology 26(4): 503–509.

    Article  Google Scholar 

  45. Torrentera, B. L. & A. G. J. Tacon, 1989. La producción de alimento vivo y su importancia en acuicultura. FAO, Brasil.

    Google Scholar 

  46. Triantaphyllidis, G. V., G. R. J. Criel, T. J. Abatzopoulos, K. M. Thomas, J. Peleman, J. A. Beardmore & P. Sorgeloos, 1997. International Study on Artemia LVII. Morphological and molecular characters suggest conspecificity of all bisexual European and North African Artemia populations. Marine Biology 129: 477–487.

    Article  CAS  Google Scholar 

  47. Triantaphyllidis, G. V., T. J. Abatzopoulos & P. Sorgeloos, 1998. Review of the biogeography of the genus Artemia (Crustacea, Anostraca). Journal of Biogeography 25: 213–226.

    Article  Google Scholar 

  48. Valverde, J. R., B. Batuecas, C. Moratilla, R. Marco & R. Garesse, 1994. The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. Journal of Molecular Evolution 39: 400–408.

    Article  CAS  Google Scholar 

  49. Van Stappen, G., 1996. Introduction biology and ecology of Artemia. In Lavens P. & P. Sorgeloos (eds), Manual on the Production and Use of Live Food for Aquaculture (FAO). Fisheries Technical Paper No 361, Rome, Italy: 101–121.

  50. Van Stappen, G., 2002. Zoogeography. In Abatzopoulos, T. J., J. A. Beardmore, J. S. Clegg & P. Sorgeloos (eds), Artemia: Basic and Applied Biology. Kluwer Academic Publishers, The Netherlands: 171–224.

    Google Scholar 

  51. Van Stappen, G., L. Y. Sui, N. H. Xin & P. Sorgeloos, 2003. Characterization of high-altitude Artemia populations from the Qinghai-Tibet Plateau, PR China. Hydrobiologia 500: 179–192.

    Article  Google Scholar 

  52. Vos, J., P. Léger, P. Vanhaecke & P. Sorgeloos, 1984. Quality evaluation of brine shrimp Artemia cysts produced in Asian Salt ponds. Hydrobiologia 108: 17–23.

    CAS  Google Scholar 

  53. Watanabe, T., F. Oowa, C. Kitajima & S. Fujita, 1980. Relationship between dietary value of brine shrimp Artemia salina and their content of ω3 highly unsaturated fatty acids. Bulletin of the Japanese Society of Scientific Fisheries 46: 35–41.

    CAS  Google Scholar 

  54. Zuñiga, O., R. Wilson, F. Amat & F. Hontoria, 1999. Distribution and characterization of Chilean populations of the brine shrimp Artemia (Crustacea, Branchiopoda, Anostraca). International Journal of Salt Lake Research 8: 23–40.

    Google Scholar 

Download references

Acknowledgements

The current work has been performed through the visits of Olga Ruiz and Dra. Alba Papeschi to the Department of Genetics, Development and Molecular Biology (Aristotle University of Thessaloniki) within the framework of the EU project ICA4-CT-2001-10020 (INCO) on Artemia biodiversity.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Olga Ruiz.

Additional information

Handling editor: K. Martens

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ruiz, O., Amat, F., Saavedra, C. et al. Genetic characterization of Argentinean Artemia species with different fatty acid profiles. Hydrobiologia 610, 223–234 (2008). https://doi.org/10.1007/s10750-008-9437-6

Download citation

Keywords

  • Artemia
  • Genetic diversity
  • Molecular markers
  • Polyunsaturated fatty acids