Skip to main content
Log in

Patterns of genetic differentiation in the Gymnogeophagus gymnogenys species complex, a neotropical cichlid from South American basins

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The neotropical cichlid genus Gymnogeophagus is distributed in the Río de la Plata basin and in Dos Patos and Merín coastal lagoons on the border between Uruguay and southern Brazil. A phylogeographic approach based on mitochondrial cytochrome b analysis was performed to assess the patterns and processes of differentiation in this taxon. Gymnogeophagus gymnogenys showed high haplotype diversity (H = 0.992) and corrected mtDNA genetic distances ranged from 0 to 5.3%. Our analyses yielded robust support for the existence of four monophyletic groups within G. gymnogenys from the analyzed basins. No correlation between the aforementioned clades and geographic structure was found, since individuals belonging to different phylogenetic clades inhabit the same locality. The phylogeographic approach presented here showed that these four phylogroups (1, 2, 3 and 4) were sister groups. Our present findings would corroborate that G. gymnogenys could be integrated by different phylogenetic lineages, showing an explosive differentiation pattern and confirming the hypothesis that this taxon constitutes a species complex.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arratia G, Cione A (1996) The record of fossil fishes of Southern South America. Muenchner Geowiss. Abh., pp 9–11

  • Barluenga M, Meyer A (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Mol Ecol 13:2061–2076

    Article  PubMed  CAS  Google Scholar 

  • Barluenga M, Stölting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723

    Article  PubMed  CAS  Google Scholar 

  • Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    Article  PubMed  CAS  Google Scholar 

  • Cantatore P, Roberti M, Pesole G, Ludovico A, Milella F, Gasaleta MN, Saccone C (1994) Evolutionary analysis of cytochrome b sequences in some Perciformes: evidence for a slower rate of evolution than in mammals. J Mol Evol 39:589–597

    Article  PubMed  CAS  Google Scholar 

  • Casciotta J, Arratia G (1993) Tertiary cichlid fishes from Argentina and reassessment of the phylogeny of New World cichlids. Kaupia 2:195–240

    Google Scholar 

  • Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) Concordance between dispersal and mitochondrial gene flow: isolation by distance in a tropical teleost, Lates calcarifer (Australian barramundi). Heredity 80:187–197

    Article  Google Scholar 

  • Durand JD, Tine M, Panfili J, Thiaw OT, Laë R (2005) Impact of glaciations and geographic distance on the genetic structure of a tropical estuarine fish, Ethmalosa fimbriata (Clupeidae, S. Bowdich, 1825). Mol Phylogenet Evol 36:277–287

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (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 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Farias IP, Ortí G, Sampaio I, Schneider H, Meyer A (1999) Mitochondrial DNA phylogeny of the family Cichlidae: monophyly and fast molecular evolution of the Neotropical assemblage. J Mol Evol 48:703–711

    Article  PubMed  CAS  Google Scholar 

  • Farias IP, Ortí G, Meyer A (2000) Total evidence: molecules, morphology, and the phylogenetics of cichlid fishes. J Exp Zool 288:76–92

    Article  PubMed  CAS  Google Scholar 

  • Farias IP, Ortí G, Sampaio I, Schneider H, Meyer A (2001) The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 53:89–103

    PubMed  CAS  Google Scholar 

  • Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fu Y-X (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Hensel RF (1870) Beiträge zur Kenntniss der wirbelthiere Südbrasiliensis. (Fortsetzung) Archiv für Naturgeschidite 36:50–91

    Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hillis DM, Mable BK, Moritz C (1996) Applications of molecular systematics. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. 2nd edn. Sinauer Associates, Sunderland, MA, pp 515–543

    Google Scholar 

  • Hulsey CD, García de León FJ, Johnson YS, Hendrickson DA, Near TJ (2004) Temporal diversification of Mesoamerican cichlid fishes across a major biogeographic boundary. Mol Phylogenet Evol 31:754–764

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    PubMed  CAS  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  PubMed  CAS  Google Scholar 

  • Kornfield IL, Smith DC, Gagnon PS, Taylor JN (1982) The cichlid fish of Cuatro Cienagas, Mexico: direct evidence of conspecificity among distinct trophic morphs. Evolution 36:658–664

    Article  Google Scholar 

  • Kullander SO (2003) Family cichlidae. In: Kullander SO, Reis R, Ferraris CJ (eds) Check list of the freshwater fishes of South and Central America. Museu de Ciências e Tecnologia, Pontificia Universidade Católica do Rio Grande do Sul. Porto Alegre, pp 605–654

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • López-Fernández H, Taphorn DC (2004) Geophagus abalios, G. dicrozoster and G. winemilleri (Perciformes: Cichlidae), three new species from Venezuela. Zootaxa 439:1–27

    Google Scholar 

  • López-Fernández H, Honeycutt RL, Winemiller KO (2005) Molecular phylogeny and evidence for an adaptive radiation of geophagine cichlids from South America (Perciformes: Labroidei). Mol Phylogenet Evol 34:227–244

    Article  PubMed  CAS  Google Scholar 

  • Malabarba LR, Isaia EA (1992) The freshwater fish fauna of the Rio Tramandaí drainage, Rio Grande do Sul, with a discussion of its local origin. Comun Mus Ciênc PUCRS Sér Zool 5:197–223

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Martin AP, Bermingham E (1998) Systematics and evolution of lower Central American cichlids inferred from analysis of cytochrome b gene sequences. Mol Phylogenet Evol 9:192–203

    Article  PubMed  CAS  Google Scholar 

  • Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43

    PubMed  CAS  Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson A (1990) Monophyletic origin of Lake Victoria fishes suggested by mitochondrial DNA sequences. Nature 347:550–553

    Article  PubMed  CAS  Google Scholar 

  • Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY, USA

    Google Scholar 

  • Palumbi S, Martin A, Romano S, McMillan WO, Stice L Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, Univ. Hawaii, Honolulu

  • Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    Article  PubMed  CAS  Google Scholar 

  • Reis RE, Malabarba LR (1988) Revision of the neotropical cichlid genus Gymnogeophagus (Ribeiro, 1918), with descriptions of two new species (Pisces, Perciformes). Revista Bra Zool 4:259–305

    Google Scholar 

  • Ribeiro AM (1918) Dos gêneros e três espécies novas de peixes Brasileiros determinados nas coleçoes do Museu Paulista. Revta Mus Paulista, Sao Paulo 10:787–791

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Roe KJ, Conkel D, Liderad C (1997) Molecular systematics of Middle American cichlid fishes and the evolution of trophic-types in ‘Cichlasoma (Amphilophus)’ and ‘C. (Thorichthys)’. Mol Phylogenet Evol 7:366–376

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messenguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Rüber L, Meyer A, Sturmbauer C, Verheyen E (2001) Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Mol Ecol 10:1207–1225

    Article  PubMed  Google Scholar 

  • Salzburger W, Mack T, Verheyen E, Meyer A (2005) Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol 5:17–32

    Article  PubMed  Google Scholar 

  • Schliewen UK, Tautz D, Pääbo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368:629–632

    Article  PubMed  CAS  Google Scholar 

  • Schliewen UK, Rassmann K, Markmann M, Markert J, Kocher T, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol 10:1471–1488

    Article  PubMed  CAS  Google Scholar 

  • Seehausen O, Witte F, van Alphen JJM, Bouton N (1998) Direct mate choice maintains diversity in among sympatric cichlids in Lake Victoria. J Fish Biol 53:37–55

    Article  Google Scholar 

  • Sprechmann P (1980) Paleoecología, paleogeografía y estratigrafía de la región costera del Uruguay durante el Neógeno y Cuartario. In: Actas II Cong. Argentino Paleont., Bioestr., y I Congr. Latinoamericano Paleont., Buenos Aires. Tomo III. pp 237–256

  • Sturmbauer C, Verheyen E, Meyer A (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern Africa. Mol Biol Evol 11:691–703

    PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Inc., Sunderland, MA

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Templeton A (2001) Using phylogeographic analyses of gene trees to test species status and processes. Mol Ecol 10:779–791

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876

    Article  PubMed  CAS  Google Scholar 

  • Verheyen E, Salzburger W, Snoeks J, Meyer A (2003) Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:325–329

    Article  PubMed  CAS  Google Scholar 

  • Weitzman SH, Menezes NA, Weitzman MJ (1988) Phylogenetic biogeography of the glandulocaudini (Teleostei, Characiformes, Characidae) with comments on the distributions of other freshwater fishes in eastern and southeast Brazil. Proceedings of the Workshop on Neotropical Distribution Patterns. Academia Brasileira de Ciências, pp 343–377

  • Wilson AB, Noack K, Meyer A (2000) Incipient speciation in sympatric Nicaraguan crater lake cichlid fishes: sexual selection vs. ecological diversification. Proc R Soc Lond Series B 267:2133–2141

    Article  CAS  Google Scholar 

  • Wimberger PH, Reis RE, Thornton KR (1998) Mitochondrial phylogenetics, biogeography, and evolution of parental care and mating systems in Gymnogeophagus (Perciformes: Cichlidae). In: Malabarba LR, Reis RE, Vari RP, Lucena ZM, Lucena CAS (eds) Phylogeny and classification of neotropical fishes. Editora Universitaria, Pontificia Universidad Católica do Río Grande do Sul, Porto Alegre, pp 509–518

  • Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354

    Google Scholar 

Download references

Acknowledgments

We wish to thank the following people: P. Laurino and Fa.Flo.Dul. organization who donated some Gymnogeophagus cf. gymnogenys and G. cf. labiatus samples; M. Loureiro and I. González who kindly provided the remaining samples and V. Gutiérrez, P. Gaiero and two anonymous reviewers for helpful suggestions for improving earlier versions of this manuscript. This research received financial support from G. García’s DT-Project (CSIC-UDELAR-Uruguay). The authors are grateful to the Japanese Government for donation of equipment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvana Pereyra.

Appendix

Appendix

  List of specimens included in this study

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pereyra, S., García, G. Patterns of genetic differentiation in the Gymnogeophagus gymnogenys species complex, a neotropical cichlid from South American basins. Environ Biol Fish 83, 245–257 (2008). https://doi.org/10.1007/s10641-008-9329-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-008-9329-7

Keywords

Navigation