Skip to main content
Log in

High Ag-NOR-site variation associated to a secondary contact in brown trout from the Iberian Peninsula

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The analysis of nucleolar organizer regions (NORs) using silver (Ag-) staining and in situ hybridization (ISH) in brown trout (Salmo trutta) from various river basins in the Iberian Peninsula revealed high variation in the number and location of NORs. A total of 17 different Ag-NOR sites were revealed in 10 different chromosome pairs. Three different Ag-NOR patterns clustered by river basins and strongly associated to the internal transcribed spacer 1 (ITS1) variation were detected. The main variability in NOR-sites was found in a secondary contact between two divergent lineages of brown trouts at Duero basin. Our results confirmed the abrupt break in the spatial distribution of genetic variation of brown trout populations previously reported at Duero basin. We hypothesize that NOR-site variation might be a consequence of hybridization between divergent lineages of brown trouts and that NORs could play a major role in the maintenance of a hybrid zone in Duero basin via post-zygotic isolation mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amemiya CT, Gold JR (1988) Chromosomal NORs as taxonomic and systematic characters in North American cyprinid fishes. Genetica 76:81–90. doi:10.1007/BF00058806

    Article  Google Scholar 

  • Arias J, Sánchez L, Martínez P (1995) Low stocking incidence in brown trout populations from Northwestern Spain monitored by LDH-5* diagnostic marker. J Fish Biol 47:170–176. doi:10.1111/j.1095-8649.1995.tb06053.x

    Article  CAS  Google Scholar 

  • Bernatchez L (2001) The evolutionary history of brown trout Salmo trutta L. inferred from phylogeographic, nested clade and mismatch analyses of mitochondrial DNA variation. Evol Int J Org Evol 55:351–379

    CAS  Google Scholar 

  • Bingham PM, Kidwell MG, Rubin GM (1982) The molecular-basis of P-M hybrid dysgenesis -the role of the P-element, a P-strain-specific transposon family. Cell 29:995–1004. doi:10.1016/0092-8674(82)90463-9

    Article  PubMed  CAS  Google Scholar 

  • Bouza C, Castro J, Sánchez L, Martínez P (2001) Allozymic evidence of parapatric differentiation of brown trout (Salmo trutta L.) within an Atlantic river basin of the Iberian Peninsula. Mol Ecol 10:1455–1469. doi:10.1046/j.1365-294X.2001.01272.x

    Article  PubMed  CAS  Google Scholar 

  • Bouza C, Vilas R, Castro J, Martínez P (2008) Mitochondrial haplotype variability of brown trout populations from Northwestern Iberian Peninsula, a secondary contact area between lineages. Conserv Genet. doi:10.1007/s10592-007-9398-8

  • Castro J, Rodríguez S, Arias J, Sánchez L, Martínez P (1994) A population analysis of Robertsonian and Ag-NOR polymorphisms in brown trout (Salmo trutta). Theor Appl Genet 89:105–111. doi:10.1007/BF00226990

    Article  Google Scholar 

  • Castro J, Viñas A, Sánchez L, Martínez P (1996) Characterization of an atypical NOR site polymorphism in brown trout (Salmo trutta) with Ag-and CMA3 staining, and fluorescence in situ hybridization. Cytogenet Cell Genet 75:234–239. doi:10.1159/000134491

    Article  PubMed  CAS  Google Scholar 

  • Castro J, De Lucchini S, Nardi I, Sánchez L, Martínez P (1997) Molecular analysis of a NOR site polymorphism in brown trout (Salmo trutta): organization of rDNA intergenic spacers. Genome 40:916–922. doi:10.1139/g97-118

    Article  PubMed  CAS  Google Scholar 

  • Castro J, Rodríguez S, Pardo BG, Sánchez L, Martínez P (2001) Population analysis of an unusual NOR-site polymorphism in brown trout (Salmo trutta L.). Heredity 86:291–302. doi:10.1046/j.1365-2540.2001.00834.x

    Article  PubMed  CAS  Google Scholar 

  • Cortey M, García-Marín JL (2002) Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic brown trout. J Fish Biol 60:1058–1063. doi:10.1111/j.1095-8649.2002.tb02429.x

    Article  CAS  Google Scholar 

  • Cortey M, Pla C, García-Marín JL (2004) Historical biogeography of Mediterranean trout. Mol Phylogenet Evol 33:831–844. doi:10.1016/j.ympev.2004.08.012

    Article  PubMed  Google Scholar 

  • Dubcovsky J, Dvörak J (1995) Ribosomal RNA multigene loci: nomads of the triticeae genomes. Genetics 140:1367–1377

    PubMed  CAS  Google Scholar 

  • Gernand D, Golczyk H, Rutten T, Ilnicki T, Houben A, Joachimiak AJ (2007) Tissue culture triggers chromosome alterations, amplification, and transposition of repeat sequences in Allium fistulosum. Genome 50:435–442. doi:10.1139/G07-023

    Article  PubMed  CAS  Google Scholar 

  • Hartley SE (1988) Cytogenetic studies of Atlantic salmon Salmo salar L., in Scotland. J Fish Biol 33:735–740. doi:10.1111/j.1095-8649.1988.tb05518.x

    Article  Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015. doi:10.1007/BF01953855

    Article  PubMed  CAS  Google Scholar 

  • Jankun M, Martínez P, Pardo BG, Kirtiklis L, Rab P, Rabova M, Sánchez L (2001) Ribosomal genes in coregonid fishes (Coregonus lavaretus, C. albula and C. peled): single and multiple nucleolar organizer regions. Heredity 87:672–679. doi:10.1046/j.1365-2540.2001.00964.x

    Article  PubMed  CAS  Google Scholar 

  • Maggini FT, Cremonini R, Zolfino C, Tucci GF, D’Ovidio R, Delre V, DePace C, Scarascia Mugnozza GT, Cionini PG (1991) Structure and chromosome localization of DNA sequences related to ribosomal subrepeats in Vicia faba. Chromosoma 100:229–234. doi:10.1007/BF00344156

    Article  PubMed  CAS  Google Scholar 

  • Mantovani M, s Abel LD, Mestriner CA, Moreira-Filho O (2000) Accentuated polymorphism of heterochromatin and nucleolar organizer regions in Astyanax scabripinnis (Pisces, Characidae): tools for understanding karyotypic evolution. Genetica 109:161–168. doi:10.1023/A:1017546601065

    Article  PubMed  CAS  Google Scholar 

  • Martínez P, Viñas A, Bouza C, Arias J, Amaro R, Sánchez L (1991) Cytogenetical characterization of hatchery stocks and natural populations of sea and brown trout from Northwestern Spain. Heredity 66:9–17. doi:10.1038/hdy.1991.2

    Article  Google Scholar 

  • Martínez P, Viñas A, Bouza C, Castro J, Sánchez L (1993) Quantitative analysis of the variability of NOR region in Salmo trutta. Genome 36:1119–1123. doi:10.1139/g93-149

    Article  PubMed  Google Scholar 

  • Martínez P, Bouza C, Castro J, Hermida M, Pardo BG, Sánchez L (2007) Analysis of a secondary contact between divergent lineages of brown trout Salmo trutta L from Duero basin using microsatellites and mtDNA RFLPs. J Fish Biol 71B:195–213. doi:10.1111/j.1095-8649.2007.01551.x

    Article  Google Scholar 

  • Nei M (1987) Molecular Evolution Genetics. Columbia University Press, New York

    Google Scholar 

  • Pardo BG, Bouza C, Castro J, Martínez P, Sánchez L (2001) Localization of ribosomal genes in pleuronectiformes using Ag-and CMA3 banding and in situ hybridization. Heredity 86:531–536. doi:10.1046/j.1365-2540.2001.00802.x

    Article  PubMed  CAS  Google Scholar 

  • Pedrosa-Harand A, Souza de Almeida CC, Mosiolek MM, Blair MW, Schweizer D, Guerra M (2006) Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet 112:924–933. doi:10.1007/s00122-005-0196-8

    Article  PubMed  CAS  Google Scholar 

  • Pendás AM, Morán P, García-Vázquez E (1993) Multichromosomal location of ribosomal RNA genes and heterochromatin association in brown trout. Chromosome Res 1:63–67. doi:10.1007/BF00710608

    Article  PubMed  Google Scholar 

  • Pérez-González CE, Eickbush TH (2001) Dynamics of R1 and R2 elements in the rDNA locus of Drosophila simulans. Genetics 158:1557–1567

    PubMed  Google Scholar 

  • Phillips RB, Pleyte KA, Hartley SE (1988) Stock-specific differences in the number and chromosome positions of the nucleolar organizer regions in Arctic charr (Salvelinus alpinus). Cytogenet Cell Genet 48:9–12. doi:10.1159/000132576

    Article  Google Scholar 

  • Presa P, Pardo BG, Martínez P, Bernatchez L (2002) Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Mol Biol Evol 19:2161–2175

    Google Scholar 

  • Raskina O, Belyayev A, Nevo E (2004) Quantum speciation in Aegilops: molecular cytogenetic evidence from rDNA cluster variability in natural population. Proc Natl Acad Sci USA 101:14818–14823. doi:10.1073/pnas.0405817101

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148. doi:10.1007/BF00328466

    Article  Google Scholar 

  • Suárez J, Bautista JM, Almodóvar A, Machordom A (2001) Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87:198–206. doi:10.1046/j.1365-2540.2001.00905.x

    Article  PubMed  Google Scholar 

  • Wilson GN, Hollar BA, Waterson JR, Schmickel RD (1978) Molecular analysis of cloned human 18S ribosomal DNA segments. Proc Natl Acad Sci USA 15:5367–5371. doi:10.1073/pnas.75.11.5367

    Article  Google Scholar 

  • Woznicki P, Martínez P, Pardo BG, Jankun M, Sánchez L (2000) A population analysis of the structure and variability of NOR of Salmo trutta by Ag, CMA3 and ISH. Genetica 108:113–118. doi:10.1023/A:1004055125295

    Article  CAS  Google Scholar 

  • Zhuo L, Reed KM, Phillips RB (1995) Hypervariability of ribosomal DNA at multiple chromosomal sites in lake trout (Salvelinus namaycush). Genome 38:487–496

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a Spanish Government grant (REN2001-3051) and by a contract with Castilla-León Government (SC-132/02). Authors are indebted with Sonia Gómez and Susana Sánchez by their technical assistance. We also wish to thank to José Luis García-Marín, Emilio Roy, Juan Carlos Velasco and Castilla-León Government for their aid in collecting samples and permission for publishing the present data, and also to all the forest guards that made the sampling possible.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Martínez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martínez, P., Castro, J., Pardo, B.G. et al. High Ag-NOR-site variation associated to a secondary contact in brown trout from the Iberian Peninsula. Genetica 136, 419–427 (2009). https://doi.org/10.1007/s10709-008-9342-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-008-9342-y

Keywords

Navigation