Advertisement

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

  • Lubomír Piálek
  • Jorge Casciotta
  • Adriana Almirón
  • Oldřich Říčan
ADVANCES IN CICHLID RESEARCH III
  • 91 Downloads

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.

Keywords

Convergence Diversification Replicated evolution Species flock 

Notes

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.

Supplementary material

10750_2018_3754_MOESM1_ESM.jpg (2.5 mb)
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)
10750_2018_3754_MOESM2_ESM.xlsx (39 kb)
Table S1. Specimens included in the study. Supplementary material 2 (XLSX 38 kb)
10750_2018_3754_MOESM3_ESM.xls (16 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)

References

  1. Alexander, D. H., J. Novembre & K. Lange, 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19: 1655–1664.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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].
  3. Barlow, G. W., 2000. The Cichlid Fishes: Nature´s Grand Experiment in Evolution. Perseus Press, New York.Google Scholar
  4. Burress, E. D., 2015. Cichlid fishes as models of ecological diversification: patterns, mechanisms, and consequences. Hydrobiologia 748: 7–27.CrossRefGoogle Scholar
  5. Burress, E. D., 2016. Ecological diversification associated with the pharyngeal jaw diversity of Neotropical cichlid fishes. Journal of Animal Ecology 85: 302–313.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. Casciotta, J. R., 1987. Crenicichla celidochilus n. sp. from Uruguay and a multivariate analysis of the lacustris group (Perciformes, Cichlidae). Copeia 1987: 883–891.CrossRefGoogle Scholar
  11. Casciotta, J. R. & G. Arratia, 1993. Jaws and teeth of American Cichlids (Pisces: Labroidei). Journal of Morphology 217: 1–36.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.Google Scholar
  14. 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.CrossRefGoogle Scholar
  15. Chifman, J. & L. Kubatko, 2014. Quartet-inference from SNP data under the coalescent model. Bioinformatics 30: 3317–3324.CrossRefPubMedPubMedCentralGoogle Scholar
  16. de Queiroz, K., 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886.CrossRefPubMedGoogle Scholar
  17. Drummond, A. J. & A. Rambaut, 2007. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ferraris, C. J., 2007. Checklist of catfishes, recent and fossil (Osteichthyes: Siluriformes), and catalogue of siluriform primary types. Zootaxa 1418: 1–628.CrossRefGoogle Scholar
  20. 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
  21. Givnish, T. J., 2015. Adaptive radiation versus ‘radiation’and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytologist 207: 297–303.CrossRefPubMedGoogle Scholar
  22. Haq, B. U., J. Hardenbol & P. R. Vail, 1987. Chronology of fluctuating sea levels since the Triassic. Science 235: 1156–1167.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Koblmüller, S., K. M. Sefc & C. Sturmbauer, 2008. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615: 5–20.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Kullander, S. O., 1986. Cichlid fishes of the Amazon River drainage of Peru. Swedish Museum of Natural History, Stockholm.Google Scholar
  30. 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
  31. 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
  32. Langmead, B. & S. L. Salzberg, 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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
  34. 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.CrossRefPubMedGoogle Scholar
  35. Mirande, J. M. & S. Koerber, 2015. Checklist of the freshwater fishes of argentina (CLOFFAR). Ichthyological Contributions of PecesCriollos 36: 1–68.Google Scholar
  36. 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
  37. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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
  40. 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.Google Scholar
  41. Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. Rambaut, A., M. A. Suchard & A. J. Drummond, 2014. Tracer v1.6. [available on internet at http://tree.bio.ed.ac.uk/software/tracer].
  44. 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
  45. Říčan, O., A. Almirón & J. Casciotta, 2017. Rediscovery of Crenicichla yaha (Teleostei: Cichlidae). Ichthyological Contributions of PecesCriollos 50: 1–8.Google Scholar
  46. 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.CrossRefGoogle Scholar
  47. Schluter, D., 2000. The Ecology of Adaptive Radiation. OUP, Oxford.Google Scholar
  48. Seehausen, O., 2015. Process and pattern in cichlid radiations–inferences for understanding unusually high rates of evolutionary diversification. New Phytologist 207: 304–312.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. Simpson, G. G., 1953. The Major Features of Evolution. Columbia University Press, New York.Google Scholar
  51. Šmilauer, P. & J. Lepš, 2014. Multivariate Analysis of Ecological Data using Canoco 5. Cambridge University Press, New York.CrossRefGoogle Scholar
  52. Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Swofford, D. L., 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4 [Computer Programme]. Sinauer Associates, Sunderland, MA.Google Scholar
  54. Takahashi, T. & E. Moreno, 2015. A RAD-based phylogenetics for Orestias fishes from Lake Titicaca. Molecular Phylogenetics and Evolution 93: 307–317.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  2. 2.División Zoología Vertebrados, Facultad de Ciencias Naturales y MuseoUNLPLa PlataArgentina
  3. 3.CIC, Comisión de Investigaciones Científicas de la Provincia de Buenos AiresLa PlataArgentina

Personalised recommendations