Skip to main content
Log in

Current and historical hybridization with differential introgression among three species of cyprinid fishes (genus Cyprinella)

  • SI - GOS
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Hybridization is common among freshwater fishes, particular among the Cyprinidae. We used two mitochondrial genes and one nuclear gene to characterize hybridization among two species pairs of Cyprinella in southwestern North America. Genalogical patterns revealed that C. lutrensis and C. venusta are currently hybridizing in several localities producing apparent F1, F2 and backcross generations, yet there was no evidence for introgression outside of local hybrid zones. Alternatively, mitochondrial haplotypes from C. lutrensis appear to have introgressed into a C. lepida population in the Nueces River completely replacing the native C. lepida haplotype. There was no evidence of introgression of nuclear DNA and there does not appear to be ongoing hybridization. The population of C. lepida from the nearby Frio River exhibits no evidence of hybridization with C. lutrensis. Thus, contact between C. lutrensis and C. venusta results in the formation of localized hybrid swarms, while contact between C. lutrensis and C. lepida has resulted in complete mitochondrial introgression in the Nueces River or no apparent hybridization in the Frio River. The three different outcomes of contact between these species illustrate the variable nature of interspecific reproductive interactions and provide an excellent system in which to better understand the factors influencing hybridization among freshwater fishes.

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
Fig. 4

Similar content being viewed by others

References

  • Aboim MA, Mavarez J, Bernatchez L, Coelho MM (2010) Introgressive hybridization between two Iberian endemic cyprinid fish: a comparison between two independent hybrid zones. J Evol Biol 23:817–828

    Google Scholar 

  • Alves MJ, Coelho MM, Collares-Pereira MJ (2001) Evolution in action through hybridization and polyploidy in an Iberian freshwater fish: a genetic review. Genetica 111:375–385

    Article  PubMed  CAS  Google Scholar 

  • Blum MJ, Walters DM, Burkhead NM, Freeman BJ, Porter BA (2010) Reproductive isolation and the expansion of an invasive hybrid swarm. Biol Invasions 12:2825–2836

    Article  Google Scholar 

  • Bolnick DI, Near TJ (2005) Tempo of post-zygotic reproductive isolation in sunfishes (Teleostei: Centrarchidae). Evolution 59:1754–1767

    PubMed  Google Scholar 

  • Broughton RE and Gold JR (2000) Phylogenetic relationships in the North American cyprinid genus Cyprinella (Actinopterygii: Cyprinidae) based on sequences of the mitochondrial ND2 and ND4L genes. Copeia 1–10

  • Campton DE (1987) Natural hybridization and introgression in fishes: Methods of detection and genetic interpretations. In: Ryman N, Utter F (eds) Populations genetics and fishery management. University of Washington Press, Seattle, pp 161–192

    Google Scholar 

  • DeMarais BD, Dowling TE, Douglas M, Minckley WL, Marsh P (1992) Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: Implications for evolution and conservation. Proc Nat Acad Sci USA 89:2747–2751

    Article  PubMed  CAS  Google Scholar 

  • Dowling TE, Childs MR (1992) Impact of hybridization on a threatened trout of the Southwestern United States. Conserv Biol 6:355–364

    Article  Google Scholar 

  • Dowling TE, Secor CL (1997) The role of hybridization in the evolutionary diversification of animals. Ann Rev Ecol Syst 28:593–619

    Article  Google Scholar 

  • Dowling TE, Smith GR, Brown WM (1989) Reproductive isolation between Notropis cornutus and Notropis chrysocephalus (family Cyprinidae): Comparison of morphology, allozymes, and mitochondrial DNA. Evolution 43:620–634

    Article  Google Scholar 

  • Dowling TE, Broughton RE, DeMarais BD (1997) Significant role for historical effects in the evolution of reproductive isolation: evidence from patterns of introgression between the cyprinid fishes, Luxilus cornutus and Luxilus chrysocephalus. Evolution 51:1574–1583

    Article  Google Scholar 

  • Echelle AA, Connor PJ (1989) Rapid, geographically extensive genetic introgression after secondary contact between two pupfish species (Cyprinodon, Cyprinodontidae). Evolution 43:717–727

    Article  Google Scholar 

  • Gerber AS, Tibbets CA, Dowling TE (2001) The role of introgressive hybridization in the evolution of the Gila robusta complex (Teleostei: Cyprinidae). Evolution 55:2028–2039

    PubMed  CAS  Google Scholar 

  • Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxf Surv Evol Biol 7:69–128

    Google Scholar 

  • Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20

    Article  Google Scholar 

  • Hubbs C (1972) A checklist of Texas freshwater fishes. Tex Parks Wildl Dept Tech Ser 11:1–11

    Google Scholar 

  • Hubbs C, Strawn K (1956) Interfertility between two sympatric fishes, Notropis lutrensis and Notropis venustus. Evolution 10:341–344

    Article  Google Scholar 

  • Jordan DS, Evermann BW (1896) The fishes of North and Middle America. Bull US Nat Hist Mus 47:1–1240

    Google Scholar 

  • Keck BP, Near TJ (2010) Geographic and temporal aspects of mitochondrial replacement in Nothonotus darters (Teleostei: Percidae: Etheostomatinae). Evolution 64:1410–1428

    PubMed  CAS  Google Scholar 

  • Lytle GL (1972) Cyprinid fishes of the subgenus Cyprinella of Notropis from southeast Texas, USA., and northeast Mexico, M.S. Thesis, Arizona State University, Tempe, AZ

  • Matthews WJ (1987) Geographic variation in Cyprinella lutrensis (Pisces: Cyprinidae) in the United States, with notes on Cyprinella lepida. Copeia 1987:616–637

    Article  Google Scholar 

  • Mayden RL (1989) Phylogenetic studies of North American minnows, with emphasis on the genus Cyprinella (Teleostei: Cypriniformes). Univ Kansas Mus Nat Hist Misc Publ 80:1–189

    Google Scholar 

  • Mayden RL, Burr BM, Page LM, Miller RR (1992) The native freshwater fishes of North America. In: Mayden RL (ed) Systematics historical ecology and North American freshwater fishes. Stanford University Press, Stanford, pp 827–863

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Richardson LR and Gold JR (1995) Evolution of the Cyprinella-Lutrensis Species-Complex .2. Systematics and Biogeography of the Edwards Plateau Shiner, Cyprinella-Lepida. Copeia 28–37

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models 19:1572–1574

  • Schmidt TR, Bielawski JP, Gold JR (1998) Molecular phylogenetics and evolutionof the cytochrome b gene in the cyprinid genus Lythrurus (Actinopterygii: Cypriniformes). Copeia 1998:14–22

    Article  Google Scholar 

  • Schonhuth S, Mayden RL (2010) Phylogenetic relationships in the genus Cyprinella (Actinopterygii: Cyprinidae) based on mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 55:77–98

    Article  PubMed  Google Scholar 

  • Scribner KT, Page KS, Bartron ML (2001) Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev fish biol fish 10:293–323

    Article  Google Scholar 

  • Smith GR (1992) Introgression in fishes significance for paleontology, cladistics, and evolutionary rates. Syst Biol 41:41–57

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • Turner BJ, Brett BH, Miller RR (1980) Interspecific hybridization and the evolutionary origin of a gynogenetic fish, Poecilia formosa. Evolution 34:917–922

    Article  Google Scholar 

  • Walters DM, Blum MJ, Rashleigh B, Freeman BJ, Porter BA, Burkhead NM (2008) Red shiner invasion and hybridization with blacktail shiner in the upper Coosa River, USA. Biol Invas 10:1229–1242

    Article  Google Scholar 

Download references

Acknowledgments

R.E.B. wishes to thank Richard G. Harrison for excellent advice and inspiration. We thank E. Marsh-Matthews, W. Matthews and P. Reneau for assistance collecting or providing specimens. All specimens were collected under the relevant permits granted by the states of Texas and Oklahoma. We thank E. Marsh-Matthews, W. Matthews, J. Gold and L. Richardson for insightful discussions about southwestern Cyprinella. The work benefited from Undergraduate Research Opportunity awards from the University of Oklahoma Honors College (to K.C.V. and L.L.R.) and award DEB-0732988 from the National Science Foundation (to R.E.B.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard E. Broughton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Broughton, R.E., Vedala, K.C., Crowl, T.M. et al. Current and historical hybridization with differential introgression among three species of cyprinid fishes (genus Cyprinella). Genetica 139, 699–707 (2011). https://doi.org/10.1007/s10709-011-9578-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9578-9

Keywords

Navigation