From shallow to deep divergences: mixed messages from Amazon Basin cichlids
Cichlids are a conspicuous component of Amazonian ichthyofauna, filling a wide range of niches. Yet taxonomy of many groups is still poorly known in the Amazon, and most of the yet-to-be discovered species are concentrated there. We analyzed 230 individuals sampled from six major Amazonian River Basins representing 56 morpho-species, 34 nominal and 22 undescribed species in 18 cichlid genera. We used four different single-locus species-discovery (SLSD) methods, delimiting between 53 (mPTP) and 57 (GMYC) species/lineages. When detected, species/lineages are hierarchically geographically structured. Many groups such as the Geophaginae and the Cichlinae have recently diversified, and species of genera such as Cichla and Symphysodon hybridize or have a history of hybridization; thus, these species will not be detected by SLSD methods. At the same time, for example, the genera Apistogramma and Biotodoma harbor cryptic species. For all these reasons, species/lineage diversity of Amazonian cichlids is significantly underestimated. The diversity of Amazonian cichlids is particularly remarkable given that the 570 species of Neotropical cichlids, many of which are from the Amazon Basin, are found in just 1.7% of the freshwater aquatic habitat in which the ~ 2,000 species of the East African rift lake cichlids evolved.
KeywordsCichlidae Cryptic diversity Cytochrome oxidase subunit I COI
We thank Lúcia Py-Daniel, Jansen Zuanon and the Ichthyology Group (Rafaela Ota, Madoka Ito, Isabela Soares, Douglas Bastos) at INPA for help with specimen identification. This study formed a portion of APCC’s Masters Dissertation in the Genetics, Conservation and Evolutionary Biology Graduate Program INPA/UFAM. Financial support was provided by CNPq Grant No. 575603/2008-9 and CNPq/SISBIOTA-BioPHAM (Grant No. CNPq 563348/2010) to IPF, and CNPq Grant No. 483155/2010-1 and 490682/2010 to TH. APCC received a Graduate Student Fellowship from CNPq, RAC a “science without borders” Postdoctoral Fellowship CNPq Grant No. 400813/2012-2, JGM a COLCIENCIAS Graduate Student Fellowship, and IPF and TH a CNPq Research Productivity Fellowships. Permission to carry out the fieldwork and the collection of tissue samples was granted by IBAMA (License No. 11325-1).
- Bleher, H., K. N. Stölting, W. Salzburger & A. Meyer, 2007. Revision of the genus Symphysodon Heckel, 1840 (Teleostei: Perciformes: Cichlidae) based on molecular and morphological characters. Aqua, Journal of Ichthyology and Aquatic Biology 12: 133–174.Google Scholar
- Drummond, A. J., B. Ashton, S. Buxton, M. Cheung, A. Cooper, C. Duran, M. Field, J. Heled, M. Kearse, S. Markowitz, R. Moir, S. Stones-Havas, S. Sturrock, T. Thierer & A. C. Wilson, 2014. Geneious v6.1.8. Biomatters, Inc., Auckland [available on internet at http://www.geneious.com/].
- Dudgeon, D., A. H. Arthington, M. O. Gessner, Z.-I. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A.-H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81: 163–182.CrossRefGoogle Scholar
- Eschmeyer, W. N., 1998. Catalog of Fishes. California Academy of Sciences Press, San Francisco.Google Scholar
- Eschmeyer, W. N. & J. D. Fong, 2018. Species by family/subfamily. CAS: Catalog of Fishes. [available on internet at http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp].
- Farias, I. P., J. P. Torrico, C. García-Dávila, M. C. F. da Santos, T. Hrbek & J.-F. Renno, 2010. Are rapids a barrier for floodplain fishes of the Amazon Basin? A demographic study of the keystone floodplain species Colossoma macropomum (Teleostei: Characiformes). Molecular Phylogenetics and Evolution 56: 1129–1135.CrossRefGoogle Scholar
- Hoorn, C., F. P. Wesselingh, H. ter Steege, M. A. Bermudez, A. Mora, J. Sevink, I. Sanmartín, A. Sanchez-Meseguer, C. L. Anderson, J. P. Figueiredo, C. Jaramillo, D. Riff, F. R. Negri, H. Hooghiemstra, J. G. Lundberg, T. Stadler, T. Särkinen & A. Antonelli, 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927–931.CrossRefGoogle Scholar
- International Energy Agency, 2013. World Energy Resources – 2013 Survey. International Energy Agency, Paris [available on internet at https://www.worldenergy.org/wp-content/uploads/2013/09/Complete_WER_2013_Survey.pdf].
- Kullander, S. O., 2003. Family Cichlidae. In Reis, R. E., S. O. Kullander & C. J. Ferraris (eds), Check List of the Freshwater Fishes of South and Central America. EDIPUCRS, Porto Alegre: 605–654.Google Scholar
- Kullander, S. O. & E. J. G. Ferreira, 2006. A review of the South American cichlid genus Cichla, with descriptions of nine new species (Teleostei: Cichlidae). Ichthyological Exploration of Freshwaters 17: 289–398.Google Scholar
- Moura, R. L., G. M. Amado-Filho, F. C. Moraes, P. S. Brasileiro, P. S. Salomon, M. M. Mahiques, A. C. Bastos, M. G. Almeida, J. M. Silva, B. F. Araujo, F. P. Brito, T. P. Rangel, B. C. V. Oliveira, R. G. Bahia, R. P. Paranhos, R. J. S. Dias, E. Siegle, A. G. Figueiredo, R. C. Pereira, C. V. Leal, E. Hajdu, N. E. Asp, G. B. Gregoracci, S. Neumann-Leitao, P. L. Yager, R. B. Francini-Filho, A. Froes, M. Campeao, B. S. Silva, A. P. B. Moreira, L. Oliveira, A. C. Soares, L. Araujo, N. L. Oliveira, J. B. Teixeira, R. A. B. Valle, C. Thompson, C. E. Rezende & F. L. Thompson, 2016. An extensive reef system at the Amazon River mouth. Science Advances 2: e1501252.CrossRefGoogle Scholar
- Piálek, L., O. Říčan, J. R. 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.CrossRefGoogle Scholar
- R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.r-project.org/].
- Rambaut, A., A. J. Drummond & M. A. Suchard, 2013. Tracer v1.6.Google Scholar
- Reis, R. E., S. O. Kullander & C. J. Ferraris Jr., 2003. Check List of the Freshwater Fishes of South and Central America. EDIPUCRS, Porto Alegre.Google Scholar
- Roxo, F. F., N. K. Lujan, V. A. Tagliacollo, B. T. Waltz, G. S. C. Silva, C. Oliveira & J. S. Albert, 2017. Shift from slow- to fast-water habitats accelerates lineage and phenotype evolution in a clade of Neotropical suckermouth catfishes (Loricariidae: Hypoptopomatinae). PLoS ONE 12: e0178240.CrossRefGoogle Scholar
- Sambrook, J. & D. Russell, 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.Google Scholar
- Shiklomanov, I. A., 1993. World fresh water resources. In Gleick, P. H. (ed.), Water in Crisis: A Guide to the World’s Fresh Water Resources. Oxford University Press, Oxford: 13–24.Google Scholar
- Sioli, H., 1984. The Amazon and its main affluents: hydrography, morphology of the river courses and river types. In Sioli, H. (ed.), The Amazon. Limnology and Landscape Ecology of a Mighty Tropical River and Its Basin. Springer, New York: 127–165.Google Scholar
- Tougard, C., C. R. García Dávila, U. Römer, F. Duponchelle, F. Cerqueira, E. Paradis, B. Guinand, C. Angulo Chávez, V. Salas, S. Quérouil, S. Sirvas & J.-F. Renno, 2017. Tempo and rates of diversification in the South American cichlid genus Apistogramma (Teleostei: Perciformes: Cichlidae). PLoS ONE 12: e0182618.CrossRefGoogle Scholar
- Venticinque, E. M., B. R. Forsberg, B. R. Barthen, P. Petry, L. Hess, A. Mercado, C. Canãs, M. Montoya, C. Durigan & M. Goulding, 2016. An explicit GIS-based river basin framework for aquatic ecosystem conservation in the Amazon. Earth System Science Data Discussions. https://doi.org/10.5194/essd-8-651-2016.CrossRefGoogle Scholar