Skip to main content
SpringerLink
Log in

A new pelagic predatory pike cichlid (Teleostei: Cichlidae: Crenicichla) from the C. mandelburgeri species complex with parallel and reticulate evolution

  • ADVANCES IN CICHLID RESEARCH III
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The Crenicichla mandelburgeri species complex from the Middle Paraná shows parallel evolution of ecomorphs to the unrelated C. missioneira species complex from the Uruguay River. In this article, we describe a new species from the C. mandelburgeri species complex that has evolved a parallel morphology and ecology to an unrelated species from the C. missioneira species complex (C. celidochilus). The new species is a pelagic predator that feeds predominantly on fishes and together with C. celidochilus is the only known pelagic species in the large riverine genus Crenicichla. The new species is endemic solely to a small tributary (the Urugua-í) of the Middle Paraná River where it is sympatric and partly syntopic with two other closely related endemic species that, however, differ strongly in their ecomorphologies (one is a generalistic invertivore and the other a specialized molluscivore). Mitochondrial DNA phylogeny finds the new species nested within the widespread C. mandelburgeri. Reduced genome-representation ddRAD analyses, however, demonstrate that this new species is of a hybrid origin and shares ancestry with C. ypo, one of the two studied sympatric species.

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

Access this article

Log in via an institution

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Alexander, D. H., J. Novembre & K. Lange, 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19: 1655–1664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews, S., 2010. FastQC. A quality control tool for high throughput sequence data. [available on internet at http://www.bioinformatics.babraham.ac.uk/projects/fastqc].

  • Barlow, G. W., 2000. The Cichlid Fishes: Nature´s Grand Experiment in Evolution. Perseus Press, New York.

    Google Scholar 

  • Burress, E. D., 2015. Cichlid fishes as models of ecological diversification: patterns, mechanisms, and consequences. Hydrobiologia 748: 7–27.

    Article  Google Scholar 

  • Burress, E. D., 2016. Ecological diversification associated with the pharyngeal jaw diversity of Neotropical cichlid fishes. Journal of Animal Ecology 85: 302–313.

    Article  PubMed  Google Scholar 

  • Burress, E. D., A. Duarte, W. S. Serra, M. Loueiro, M. M. Gangloff & L. Siefferman, 2013. Functional diversification within a predatory species flock. PLoS ONE 8: e80929.

    Article  PubMed  PubMed Central  Google Scholar 

  • Burress, E. D., A. Duarte, W. S. Serra & M. Loureiro, 2015. Rates of piscivory predict pharyngeal jaw morphology in a piscivorous lineage of cichlid fishes. Ecology of Freshwater Fish 25: 590–598.

    Article  Google Scholar 

  • Burress, E. D., F. Alda, A. Duarte, M. Loureiro, J. W. Armbruster & P. Chakrabarty, 2018a. Phylogenomics of pike cichlids (Cichlidae: Crenicichla): the rapid ecological speciation of an incipient species flock. Journal of Evolutionary Biology 31: 14–30.

    Article  CAS  PubMed  Google Scholar 

  • Burress, E. D., L. Piálek, J. Casciotta, A. Almirón, M. Tan, J. W. Armbruster & O. Říčan, 2018b. Island- and lake-like parallel adaptive radiations replicated in rivers. Proceedings of the Royal Society B 285: 20171762.

    Article  PubMed  PubMed Central  Google Scholar 

  • Casciotta, J. R., 1987. Crenicichla celidochilus n. sp. from Uruguay and a multivariate analysis of the lacustris group (Perciformes, Cichlidae). Copeia 1987: 883–891.

    Article  Google Scholar 

  • Casciotta, J. R. & G. Arratia, 1993. Jaws and teeth of American Cichlids (Pisces: Labroidei). Journal of Morphology 217: 1–36.

    Article  PubMed  Google Scholar 

  • Casciotta, J., A. Almirón, L. Piálek, S. Gómez & O. Říčan, 2010. Crenicichla ypo (Teleostei: Cichlidae), a new species from the middle Paraná basin in Misiones, Argentina. Neotropical Ichthyology 8: 643–648.

    Article  Google Scholar 

  • Catchen, J. M., A. Amores, P. Hohenlohe, W. Cresko & J. H. Postlethwait, 2011. Stacks: building and genotyping loci de novo from short-read sequences. Bethesda 1: 171–182.

    CAS  Google Scholar 

  • Chakrabarty, P., M. Warren, L. M. Page & C. C. Baldwin, 2013. GenSeq: an updated nomenclature and ranking for genetic sequences from type and non-type sources. Zookeys 346: 29–41.

    Article  Google Scholar 

  • Chifman, J. & L. Kubatko, 2014. Quartet-inference from SNP data under the coalescent model. Bioinformatics 30: 3317–3324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Queiroz, K., 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886.

    Article  PubMed  Google Scholar 

  • Drummond, A. J. & A. Rambaut, 2007. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferraris, C. J., 2007. Checklist of catfishes, recent and fossil (Osteichthyes: Siluriformes), and catalogue of siluriform primary types. Zootaxa 1418: 1–628.

    Article  Google Scholar 

  • Fryer, G. & T. D. Iles, 1972. The Cichlid fishes of the Great Lakes of Africa: their biology and evolution. T.F.H. Publications, New Jersey.

    Google Scholar 

  • Givnish, T. J., 2015. Adaptive radiation versus ‘radiation’and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytologist 207: 297–303.

    Article  PubMed  Google Scholar 

  • Haq, B. U., J. Hardenbol & P. R. Vail, 1987. Chronology of fluctuating sea levels since the Triassic. Science 235: 1156–1167.

    Article  CAS  PubMed  Google Scholar 

  • Jones, J. C., S. Fan, P. Franchini, M. Schartl & A. Meyer, 2013. The evolutionary history of Xiphophorus fish and their sexually selected sword: a genome-wide approach using restriction site-associated DNA sequencing. Molecular Ecology 22: 2986–3001.

    Article  CAS  PubMed  Google Scholar 

  • Joyce, D. A., D. H. Lunt, R. Bills, G. F. Turner, C. Katongo, N. Duftner, C. Sturmbauer & O. Seehausen, 2005. An extant cichlid fish radiation emerged in an extinct Pleistocene lake. Nature 435: 90–95.

    Article  CAS  PubMed  Google Scholar 

  • Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes & A. Drummond, 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koblmüller, S., K. M. Sefc & C. Sturmbauer, 2008. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615: 5–20.

    Article  Google Scholar 

  • Kullander, S. O., 1981. Cichlid fishes from the La Plata basin. Part I. Collections from Paraguay in the Muséum d’Histoire naturelle de Genève. Revue Suisse De Zoologie 88: 675–692.

    Article  Google Scholar 

  • Kullander, S. O., 1982. Cichlid fishes from the La Plata basin. Part III. The Crenicichla lepidota species group. Revue Suisse De Zoologie 89: 627–661.

    Article  Google Scholar 

  • Kullander, S. O., 1986. Cichlid fishes of the Amazon River drainage of Peru. Swedish Museum of Natural History, Stockholm.

    Google Scholar 

  • Kullander, S. O., 1996. Heroina isonycterina, a new genus and species of cichlid fish from Western Amazonia, with comments on cichlasomine sys-tematics. Ichthyological Exploration of Freshwaters 7: 149–172.

    Google Scholar 

  • Kullander, S. O., 2009. Crenicichla mandelburgeri, a new species of cichlid fish (Teleostei: Cichlidae) from the Paraná river drainage in Paraguay. Zootaxa 2006: 41–50.

    Google Scholar 

  • Langmead, B. & S. L. Salzberg, 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucena, C. A. S. & S. O. Kullander, 1992. The Crenicichla (Teleostei: Cichlidae) species of the Uruguai River drainage in Brazil. Ichthyological Exploration of Freshwaters 3: 97–160.

    Google Scholar 

  • Matschiner, M., Z. Musilová, J. M. Barth, Z. Starostová, W. Salzburger, M. Steel & R. Bouckaert, 2017. Bayesian phylogenetic estimation of clade ages supports trans-atlantic dispersal of cichlid fishes. Systematic Biology 66: 3–22.

    Article  PubMed  Google Scholar 

  • Mirande, J. M. & S. Koerber, 2015. Checklist of the freshwater fishes of argentina (CLOFFAR). Ichthyological Contributions of PecesCriollos 36: 1–68.

    Google Scholar 

  • Musilová, Z., O. Říčan, Š. Říčanová, P. Janšta, O. Gahura & J. Novák, 2015. Phylogeny and historical biogeography of trans-Andean cichlid fishes (Teleostei: Cichlidae). Vertebrate Zoology 65: 333–350.

    Google Scholar 

  • Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher & H. E. Hoekstra, 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7: e37135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piálek, L., O. Říčan, J. Casciotta, A. Almirón & J. Zrzavý, 2012. Multilocus phylogeny of Crenicichla (Teleostei: Cichlidae), with biogeography of the C. lacustris group: species flocks as a model for sympatric speciation in rivers. Molecular Phylogenetics and Evolution 62: 46–61.

    Article  PubMed  Google Scholar 

  • Piálek, L., K. Dragová, J. Casciotta, A. Almirón & O. Říčan, 2015. Description of two new species of Crenicichla (Teleostei: Cichlidae) from the lower Iguazú River with a taxonomic reappraisal of C. iguassuensis, C. tesay and C. yaha. Historia Natural Tercera Serie 5: 5–27.

    Google Scholar 

  • Piálek, L., E. Burress, K. Dragová, A. Almirón, J. Casciotta & O. Říčan, 2018. Phylogenomics of pike cichlids (Cichlidae: Crenicichla) of the C. mandelburgeri species complex: rapid ecological speciation in the Iguazú River and high endemism in the Middle Paraná basin. Hydrobiologia in Press.

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Purcell, S., B. Neale, K. Todd-Brown, L. Thomas, M. A. Ferreira, D. Bender, J. Maller, P. Sklar, P. I. de Bakker, M. J. Daly & P. C. Sham, 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics 81: 559–575.

    Article  CAS  PubMed  Google Scholar 

  • Rambaut, A., M. A. Suchard & A. J. Drummond, 2014. Tracer v1.6. [available on internet at http://tree.bio.ed.ac.uk/software/tracer].

  • Říčan, O., L. Piálek, K. Dragová & J. Novák, 2016. Diversity and evolution of the Middle American cichlid fishes (Teleostei: Cichlidae) with revised classification. Vertebrate Zoology 66: 1–102.

    Google Scholar 

  • Říčan, O., A. Almirón & J. Casciotta, 2017. Rediscovery of Crenicichla yaha (Teleostei: Cichlidae). Ichthyological Contributions of PecesCriollos 50: 1–8.

    Google Scholar 

  • Říčan, O., Š. Říčanová, K. Dragová, L. Piálek, A. Almirón & J. Casciotta, 2018. Species diversity in Gymnogeophagus (Teleostei: Cichlidae) and comparative biogeography of cichlids in the Middle Paraná basin, an emerging hotspot of fish endemism. Hydrobiologia in Press. https://doi.org/10.1007/s10750-018-3691-z.

    Article  Google Scholar 

  • Schluter, D., 2000. The Ecology of Adaptive Radiation. OUP, Oxford.

    Google Scholar 

  • Seehausen, O., 2015. Process and pattern in cichlid radiations–inferences for understanding unusually high rates of evolutionary diversification. New Phytologist 207: 304–312.

    Article  PubMed  Google Scholar 

  • Seehausen, O., P. J. Mayhew & J. J. M. Van Alphen, 1999. Evolution of colour patterns in East African cichlid fish. Journal of Evolutionary Biology 12: 514–534.

    Article  Google Scholar 

  • Simpson, G. G., 1953. The Major Features of Evolution. Columbia University Press, New York.

    Google Scholar 

  • Šmilauer, P. & J. Lepš, 2014. Multivariate Analysis of Ecological Data using Canoco 5. Cambridge University Press, New York.

    Book  Google Scholar 

  • Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swofford, D. L., 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4 [Computer Programme]. Sinauer Associates, Sunderland, MA.

  • Takahashi, T. & E. Moreno, 2015. A RAD-based phylogenetics for Orestias fishes from Lake Titicaca. Molecular Phylogenetics and Evolution 93: 307–317.

    Article  PubMed  Google Scholar 

  • Takahashi, T., N. Nagata & T. Sota, 2014. Application of RAD-based phylogenetics to complex relationships among variously related taxa in a species flock. Molecular Phylogenetics and Evolution 80: 137–144.

    Article  PubMed  Google Scholar 

  • Taylor, W. R. & G. C. Van Dyke, 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium 9: 107–119.

    Google Scholar 

Download references

Acknowledgements

The authors thank Soledad Gouric for the pictures of the LPJ and the authorities of Ministerio de Ecología y Recursos Naturales Renovables de la Provincia de Misiones for awarding fishing permits. We are very grateful to Vladimír Beneš, Bianka Baying, and the EMBL Genomic Core Facility in Heidelberg (Germany) for their kind advice and technical support during the DNA library finalization and Illumina sequencing. Financial support was provided by the Czech Science Foundation (GAČR) under Grant Number 14-28518P to LP; by Comisión de Investigaciones Científicas de la provincia de Buenos Aires (CIC); Facultad de Ciencias Naturales y Museo (UNLP); and Administración de Parques Nacionales. The access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum provided under the program “Projects of Large Infrastructure for Research, Development, and Innovations” (LM2010005) was highly appreciated, as well as the access to the CERIT-SC computing and storage facilities provided under the program Center CERIT Scientific Cloud, part of the Operational Program Research and Development for Innovations, Reg. No. CZ. 1.05/3.2.00/08.0144.

Author information

Authors and Affiliations

  1. Department of Zoology, Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, Ceske Budejovice, Czech Republic

    Lubomír Piálek & Oldřich Říčan

  2. División Zoología Vertebrados, Facultad de Ciencias Naturales y Museo, UNLP, Paseo del Bosque, 1900, La Plata, Buenos Aires, Argentina

    Jorge Casciotta & Adriana Almirón

  3. CIC, Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, La Plata, Buenos Aires, Argentina

    Jorge Casciotta

Authors
  1. Lubomír Piálek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Casciotta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adriana Almirón
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oldřich Říčan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oldřich Říčan.

Additional information

Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research III: Behavior, Ecology and Evolutionary Biology

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1.

Localities of C. yjhui. A) type locality, Urugua-í reservoir at camping, Misiones, Argentina (25°52′29.1″S–54°33′02.2″W). B) paratype locality, Urugua-í reservoir opposite Policia Fluvial Station (25°54′02.2″S, 54°33′18.6″W); C) paratype locality, arroyo Falso Urugua-í (25°58′26″S, 54°15′29″W). Supplementary material 1 (JPEG 2549 kb)

Table S1.

Specimens included in the study. Supplementary material 2 (XLSX 38 kb)

Table S2.

Summary of SVDQ analyses under different parameter settings with focus on relationships of C. yjhui. We have analyzed matrices with 50% and 70% SNPs, with Stacks depth of 3 and 8, and with inclusion of homozygotic, homozygotic + heterozygotic, 1st only SNP homozygotic + heterozygotic and all. The placement of sister-species relationship either with C. mandelburgeri or C. ypo is randomly distributed across the matrices. Note that in all cases support for placement with the respective species (either with C. mandelburgeri or C. ypo) is 100% in bootstrap analyses. Supplementary material 3 (XLS 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Piálek, L., Casciotta, J., Almirón, A. et al. A new pelagic predatory pike cichlid (Teleostei: Cichlidae: Crenicichla) from the C. mandelburgeri species complex with parallel and reticulate evolution. Hydrobiologia 832, 377–395 (2019). https://doi.org/10.1007/s10750-018-3754-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3754-1

Keywords

Search

Navigation