Distinguishing species of European sturgeons Acipenser spp. using microsatellite allele sequences

Journal of Fish Biology

Volumn 78, Issue 1, 2011, Pages 208-226

  Chassaing, O ^a,b   Hanni C ^b   Berrebi, P ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Flanking region; Hybridization; Specific discrimination

Indexed keywords

ACIPENSER; ACIPENSER NACCARII; ACIPENSER OXYRINCHUS; ACIPENSER STURIO; ACIPENSERIDAE;

EID: 78651440940     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2010.02852.x     Document Type: Article

References (53)

1. Abi-Rached, L., Gilles, A., Shiina, T., Pontarotti, P. & Inoko, H. (2002). Evidence of en bloc duplication in vertebrate genomes. Nature Genetics 31, 100-105.
2. Allendorf, F. W., Leary, R. F., Spruell, P. & Wenburg, J. K. (2001). The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution 16, 613-622.
3. Arlati, G. & Poliakova, L. (2009). Restoration of Adriatic sturgeon (Acipenser naccarii) in Italy: situation and perspectives. In Biology, Conservation and Sustainable Development of Sturgeons (Carmona, R., Domezain, A., Garcia-Gallego, M., Hernando, J. A., Rodriguez, F. & RuizRejon, M., eds), pp. 237-245. Dordrecht: Springer.
4. Artyukhin, E. & Vecsei, P. (1999). On the status of Atlantic sturgeon: conspecificity of European Acipenser sturio and North American Acipenser oxyrinchus. Journal of Applied Ichthyology 15, 35-37.
5. Billard, R. & Lecointre, G. (2001). Biology and conservation of sturgeon and paddlefish. Reviews in Fish Biology and Fisheries 10, 355-392.
6. Birstein, V. & Doukakis, P. (2000). Molecular analysis of Acipenser sturio L., 1758 and Acipenser oxyrinchus Mitchill, 1815: a review. Boletin Instituto Espagnol De Oceanografia 16, 61-73.
7. Birstein, V. J., Hanner, R. & DeSalle, R. (1997). Phylogeny of the Acipenseriformes: cytogenetic and molecular approaches. Environmental Biology of Fishes 48, 127-156.
8. Dawid, I. B. & Blackler, A. W. (1972). Maternal and cytoplasmic inheritance of mitochondrial-DNA in Xenopus. Developmental Biology 29, 152-161.
9. De la Herran, R., Robles, F., Martinez-Espin, E., Lorente, J. A., Rejon, C. R., Garrido-Ramos, M. A. & Rejon, M. R. (2004). Genetic identification of western Mediterranean sturgeons and its implication for conservation. Conservation Genetics 5, 545-551.
10. DeSalle, R. & Birstein, V. J. (1996). PCR identification of black caviar. Nature 381, 197-198.
11. Doukakis, P., Birstein, V. J., DeSalle, R., Ludwig, A. N., Ludwig, A., Machordom, A., Almodovar, A. & Elvira, B. (2000). Failure to confirm previous identification of two putative museum specimens of the Atlantic sturgeon, Acipenser sturio, as the Adriatic sturgeon, A-naccarii. Marine Biology 136, 373-377.
12. Elvira, B. & Almodovar, A. (1999). A morphological study of native sturgeon Acipenser sturio in Spain, and recent records of exotic siberian sturgeon. Journal of Applied Ichthyology 15, 278-279.
13. Fontana, F. (1994). Chromosomal nucleolar organizer regions in four sturgeon species as markers of karyotype evolution in Acipenseriformes (Pisces). Genome 37, 888-892.
14. Fontana, F. (2002). A cytogenetic approach to the study of taxonomy and evolution in sturgeons. Journal of Applied Ichthyology 18, 226-233.
15. Fontana, F., Tagliavini, J. & Congiu, L. (2001). Sturgeon genetics and cytogenetics: recent advancements and perspectives. Genetica 111, 359-373.
16. Forlani, A., Fontana, F. & Congiu, L. (2008). Isolation of microsatellite loci from the endemic and endangered Adriatic sturgeon (Acipenser naccarii). Conservation Genetics 9, 461-463.
17. Garrido-Ramos, M. A., Soriguer, M. C., de la Herran, R., Jamilena, M., Rejon, C. R., Domezain, A., Hernando, J. A. & Rejon, M. R. (1997). Morphometric and genetic analysis as proof of the existence of two sturgeon species in the Guadalquivir River. Marine Biology 129, 33-39.
18. Henderson-Arzapalo, A. & King, T. L. (2002). Novel microsatellite markers for Atlantic sturgeon (Acipenser oxyrinchus) population delineation and broodstock management. Molecular Ecology Notes 2, 437-439.
19. Jenneckens, I., Meyer, J. N., Horstgen-Schwark, G., May, B., Debus, L., Wedekind, H. & Ludwig, A. (2001). A fixed allele at microsatellite locus LS-39 exhibiting species-specificity for the black caviar producer Acipenser stellatus. Journal of Applied Ichthyology 17, 39-42.
20. King, T. L., Lubinski, B. A. & Spidle, A. P. (2001). Microsatellite DNA variation in Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) and cross-species amplification in the Acipenseridae. Conservation Genetics 2, 103-119.
21. Krieger, J., Hett, A. K., Fuerst, P. A., Birstein, V. J. & Ludwig, A. (2006). Unusual intraindividual variation of the nuclear 18S rRNA gene is widespread within the acipenseridae. Journal of Heredity 97, 218-225.
22. Litt, M., Hauge, X. & Sharma, V. (1993). Shadow bands seen when typing polymorphic dinucleotide repeats - some causes and cures. Biotechniques 15, 280-284.
23. Ludwig, A., Belfiore, N. M., Pitra, C., Svirsky, V. & Jenneckens, I. (2001). Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics 158, 1203-1215.
24. Ludwig, A., Debus, L., Lieckfeldt, D., Wirgin, I., Benecke, N., Jenneckens, I., Williot, P., Waldman, J. R. & Pitra, C. (2002). When the American sea sturgeon swam east - a colder Baltic Sea greeted this fish from across the Atlantic Ocean in the Middle Ages. Nature 419, 447-448.
25. Ludwig, A., Arndt, U., Lippold, S., Benecke, N., Debus, L., King, T. L. & Matsumura, S. (2008). Tracing the first steps of American sturgeon pioneers in Europe. BMC Evolutionary Biology 8, 221.
26. Ludwig, A., Arndt, U., Debus, L., Rosello, E. & Morales, A. (2009a). Ancient mitochondrial DNA analyses of Iberian sturgeons. Journal of Applied Ichthyology 25, 5-9.
27. Ludwig, A., Lippold, S., Debus, L. & Reinartz, R. (2009b). First evidence of hybridization between endangered sterlets (Acipenser ruthenus) and exotic Siberian sturgeons (Acipenser baerii) in the Danube River. Biological Invasions 11, 753-760.
28. Lynch, M. (1990). The similarity index and DNA fingerprinting. Molecular Biology and Evolution 7, 478-484.
29. May, B., Krueger, C. C. & Kincaid, H. L. (1997). Genetic variation at microsatellite loci in sturgeon: primer sequence homology in Acipenser and Scaphirhynchus. Canadian Journal of Fisheries and Aquatic Sciences 54, 1542-1547.
30. McQuown, E. C., Sloss, B. L., Sheehan, R. J., Rodzen, J., Tranah, G. J. & May, B. (2000). Microsatellite analysis of genetic variation in sturgeon: new primer sequences for Scaphirhynchus and Acipenser. Transactions of the American Fisheries Society 129, 1380-1388.
31. McQuown, E., Krueger, C. C., Kincaid, H. L., Gall, G. A. E. & May, B. (2003). Genetic comparison of lake sturgeon populations: differentiation based on allelic frequencies at seven microsatellite loci. Journal of Great Lakes Research 29, 3-13.
32. Ohno, S. (1970). Evolution by Gene Duplication. New York, NY: Springer.
33. Pages, M., Desse-Berset, N., Tougard, C., Brosse, L., Hanni, C. & Berrebi, P. (2009). Historical presence of the sturgeon Acipenser sturio in the Rhone basin determined by the analysis of ancient DNA cytochrome b sequences. Conservation Genetics 10, 217-224.
34. Peakall, R., Gilmore, S., Keys, W., Morgante, M. & Rafalski, A. (1998). Cross-species amplification of soybean (Glycine max) simple sequence repeats (SSRs) within the genus and other legume genera: implications for the transferability of SSRs in plants. Molecular Biology and Evolution 15, 1275-1287.
35. Peng, Z. G., Ludwig, A., Wang, D. Q., Diogo, R., Wei, Q. W. & He, S. P. (2007). Age and biogeography of major clades in sturgeons and paddlefishes (Pisces Acipenseriformes). Molecular Phylogenetics and Evolution 42, 854-862.
36. Presa, P. & Guyomard, R. (1996). Conservation of microsatellites in three species of salmonids. Journal of Fish Biology 49, 1326-1329.
37. Primmer, C. R., Moller, A. P. & Ellegren, H. (1996). A wide-range survey of cross-species microsatellite amplification in birds. Molecular Ecology 5, 365-378.
38. Rhymer, J. M. & Simberloff, D. (1996). Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27, 83-109.
39. Robles, F., de la Herran, R., Ludwig, A., Rejon, C. R., Rejon, M. R. & Garrido-Ramos, M. A. (2004). Evolution of ancient satellite DNAs in sturgeon genomes. Gene 338, 133-142.
40. Robles, F., de la Herran, R., Ludwig, A., Rejon, C. R., Rejon, M. R. & Garrido-Ramos, M. A. (2005). Genomic organization and evolution of the 5S ribosomal DNA in the ancient fish sturgeon. Genome 48, 18-28.
41. Schlotterer, C. & Tautz, D. (1992). Slippage synthesis of simple sequence DNA. Nucleic Acids Research 20, 211-215.
42. Sefc, K. M., Regner, F., Turetschek, E., Glossl, J. & Steinkellner, H. (1999). Identification of microsatellite sequences in Vitis riparia and their applicability for genotyping of different Vitis species. Genome 42, 367-373.
43. Tiedemann, R., Moll, K., Paulus, K. B., Scheer, M., Williot, P., Bartel, R., Gessner, J. & Kirschbaum, F. (2007). Atlantic sturgeons (Acipenser sturio, Acipenser oxyrinchus): American females successful in Europe. Naturwissenschaften 94, 213-217.
44. Tranah, G., Campton, D. E. & May, B. (2004). Genetic evidence for hybridization of pallid and shovelnose sturgeon. Journal of Heredity 95, 474-480.
45. Venkatesh, B., Ning, Y. & Brenner, S. (1999). Late changes in spliceosomal introns define clades in vertebrate evolution. Proceedings of the National Academy of Sciences of the United States of America 96, 10267-10271.
46. Walsh, P. S., Metzger, D. A. & Higuchi, R. (1991). Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506-513.
47. Williot, P., Rochard, E., Castelnaud, G., Rouault, T., Brun, R., Lepage, M. & Elie, P. (1997). Biological characteristics of European Atlantic sturgeon, Acipenser sturio, as the basis for a restoration program in France. Environmental Biology of Fishes 48, 359-372.
48. Wirgin, I., Waldman, J., Stabile, J., Lubinski, B. & King, T. (2002). Comparison of mitochondrial DNA control region sequence and microsatellite DNA analyses in estimating population structure and gene flow rates in Atlantic sturgeon Acipenser oxyrinchus. Journal of Applied Ichthyology 18, 313-319.
49. Zane, L., Patarnello, T., Ludwig, A., Fontana, F. & Congiu, L. (2002). Isolation and characterization of microsatellites in the Adriatic sturgeon (Acipenser naccarii). Molecular Ecology Notes 2, 586-588.
50. Zardoya, R., Vollmer, D. M., Craddock, C., Streelman, J. T., Karl, S. & Meyer, A. (1996). Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proceedings of the Royal Society B 263, 1589-1598.
51. Belkhir, K., Borsa, P., Goudet, J., Chikhi, L. & Bonhomme, F. (1998). Genetix, logiciel sous WindowsTM pour la génétique des populations Available at
52. Drummond, A. J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2009). Geneious v4.8 Available at
53. IUCN (2010). International Union for Conservation of Nature Red List of Threatened Species. Version 2010.1 Available at