Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Aug 22;267(1453):1687–1697. doi: 10.1098/rspb.2000.1196

Origin, radiation, dispersion and allopatric hybridization in the chub Leuciscus cephalus.

J D Durand 1, E Unlü 1, I Doadrio 1, S Pipoyan 1, A R Templeton 1
PMCID: PMC1690721  PMID: 11467433

Abstract

The phylogenetic relationships of 492 chub (Leuciscus cephalus) belonging to 89 populations across the species' range were assessed using 600 base pairs of cytochrome b. Furthermore, nine species belonging to the L. cephalus complex were also analysed (over the whole cytochrome b) in order to test potential allopatric hybridization with L. cephalus sensu stricto (i.e. the chub). Our results show that the chub includes four highly divergent lineages descending from a quick radiation that took place three million years ago. The geographical distribution of these lineages and results of the nested clade analysis indicated that the chub may have originated from Mesopotamia. Chub radiation probably occurred during an important vicariant event such as the isolation of numerous Turkish river systems, a consequence of the uplift of the Anatolian Plateau (formerly covered by a broad inland lake). Dispersion of these lineages arose from the changes in the European hydrographic network and, thus, the chub and endemic species of the L. cephalus complex met by secondary contacts. Our results show several patterns of introgression, from Leuciscus lepidus fully introgressed by chub mitochondrial DNA to Leuciscus borysthenicus where no introgression at all was detected. We assume that these hybridization events might constitute an important evolutionary process for the settlement of the chub in new environments in the Mediterranean area.

Full Text

The Full Text of this article is available as a PDF (489.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Avise J. C., Neigel J. E., Arnold J. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol. 1984;20(2):99–105. doi: 10.1007/BF02257369. [DOI] [PubMed] [Google Scholar]
  2. Avise J. C., Saunders N. C. Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics. 1984 Sep;108(1):237–255. doi: 10.1093/genetics/108.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Avise J. C., Walker D. Species realities and numbers in sexual vertebrates: perspectives from an asexually transmitted genome. Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):992–995. doi: 10.1073/pnas.96.3.992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Briolay J., Galtier N., Brito R. M., Bouvet Y. Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Mol Phylogenet Evol. 1998 Feb;9(1):100–108. doi: 10.1006/mpev.1997.0441. [DOI] [PubMed] [Google Scholar]
  5. Brito R. M., Briolay J., Galtier N., Bouvet Y., Coelho M. M. Phylogenetic relationships within genus Leuciscus (Pisces, Cyprinidae) in Portuguese fresh waters, based on mitochondrial DNA cytochrome b sequences. Mol Phylogenet Evol. 1997 Dec;8(3):435–442. doi: 10.1006/mpev.1997.0429. [DOI] [PubMed] [Google Scholar]
  6. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carmona J. A., Sanjur O. I., Doadrio I., Machordom A., Vrijenhoek R. C. Hybridogenetic reproduction and maternal ancestry of polyploid Iberian fish: the Tropidophoxinellus alburnoides complex. Genetics. 1997 Jul;146(3):983–993. doi: 10.1093/genetics/146.3.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Durand J. D., Persat H., Bouvet Y. Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol Ecol. 1999 Jun;8(6):989–997. doi: 10.1046/j.1365-294x.1999.00654.x. [DOI] [PubMed] [Google Scholar]
  9. Durand J. D., Templeton A. R., Guinand B., Imsiridou A., Bouvet Y. Nested clade and phylogeographic analyses of the chub, Leuciscus cephalus (Teleostei, cyprinidae), in Greece: implications for Balkan Peninsula biogeography. Mol Phylogenet Evol. 1999 Dec;13(3):566–580. doi: 10.1006/mpev.1999.0671. [DOI] [PubMed] [Google Scholar]
  10. Duvernell D. D., Aspinwall N. Introgression of Luxilus cornutus mtDNA into allopatric populations of Luxilus chrysocephalus (Teleostei: Cyprinidae) in Missouri and Arkansas. Mol Ecol. 1995 Apr;4(2):173–181. doi: 10.1111/j.1365-294x.1995.tb00206.x. [DOI] [PubMed] [Google Scholar]
  11. Galtier N., Gouy M., Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 1996 Dec;12(6):543–548. doi: 10.1093/bioinformatics/12.6.543. [DOI] [PubMed] [Google Scholar]
  12. Gilles A., Lecointre G., Faure E., Chappaz R., Brun G. Mitochondrial phylogeny of the European cyprinids: implications for their systematics, reticulate evolution, and colonization time. Mol Phylogenet Evol. 1998 Aug;10(1):132–143. doi: 10.1006/mpev.1997.0480. [DOI] [PubMed] [Google Scholar]
  13. Guthrie R. D. Bison evolution and zoogeography in North America during the Pleistocene. Q Rev Biol. 1970 Mar;45(1):1–15. doi: 10.1086/406360. [DOI] [PubMed] [Google Scholar]
  14. Hey J., Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. doi: 10.1093/genetics/145.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johns G. C., Avise J. C. A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol. 1998 Nov;15(11):1481–1490. doi: 10.1093/oxfordjournals.molbev.a025875. [DOI] [PubMed] [Google Scholar]
  16. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  17. Kocher T. D., Thomas W. K., Meyer A., Edwards S. V., Päbo S., Villablanca F. X., Wilson A. C. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6196–6200. doi: 10.1073/pnas.86.16.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Quesada H., Wenne R., Skibinski D. O. Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol Biol Evol. 1999 May;16(5):655–665. doi: 10.1093/oxfordjournals.molbev.a026148. [DOI] [PubMed] [Google Scholar]
  19. Rozas J., Rozas R. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 1997 Jun;13(3):307–311. [PubMed] [Google Scholar]
  20. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  21. Shaw K. L. A nested analysis of song groups and species boundaries in the Hawaiian cricket genus Laupala. Mol Phylogenet Evol. 1999 Mar;11(2):332–341. doi: 10.1006/mpev.1998.0558. [DOI] [PubMed] [Google Scholar]
  22. Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
  23. Templeton A. R., Boerwinkle E., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics. 1987 Oct;117(2):343–351. doi: 10.1093/genetics/117.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Templeton A. R. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol. 1998 Apr;7(4):381–397. doi: 10.1046/j.1365-294x.1998.00308.x. [DOI] [PubMed] [Google Scholar]
  25. Templeton A. R., Routman E., Phillips C. A. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics. 1995 Jun;140(2):767–782. doi: 10.1093/genetics/140.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Templeton A. R., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics. 1993 Jun;134(2):659–669. doi: 10.1093/genetics/134.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Waters J. M., Burridge C. P. Extreme intraspecific mitochondrial DNA sequence divergence in Galaxias maculatus (Osteichthys: Galaxiidae), one of the world's most widespread freshwater fish. Mol Phylogenet Evol. 1999 Feb;11(1):1–12. doi: 10.1006/mpev.1998.0554. [DOI] [PubMed] [Google Scholar]
  28. Zardoya R., Doadrio I. Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol. 1999 Aug;49(2):227–237. doi: 10.1007/pl00006545. [DOI] [PubMed] [Google Scholar]
  29. Zardoya R., Doadrio I. Phylogenetic relationships of Iberian cyprinids: systematic and biogeographical implications. Proc Biol Sci. 1998 Jul 22;265(1403):1365–1372. doi: 10.1098/rspb.1998.0443. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary data file
11467433s01.pdf (78.6KB, pdf)

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES