From taxonomic deflation to newly detected cryptic species: Hidden diversity in a widespread African squeaker catfish

. 2019 Oct 31 ; 9 (1) : 15748. [epub] 20191031

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31673053
Odkazy

PubMed 31673053
PubMed Central PMC6823466
DOI 10.1038/s41598-019-52306-2
PII: 10.1038/s41598-019-52306-2
Knihovny.cz E-zdroje

Cryptic genetic diversity and erroneous morphological species determination represent frequent problems in biodiversity research. Here, examination of 138 specimens of Synodontis (Mochokidae, Siluriformes) from the Nile River and Lake Turkana revealed the presence of both S. schall-like and S. frontosus-like morphotypes, with a phenotypic gradient between them. We concluded phylogenetic and population genetic analyses based on two mitochondrial and one nuclear marker including 131 coxI (565 bp), 96 cytb (973 bp) and 19 RAG2 (896 bp) sequences from the Nile-Turkana population, plus additional GenBank data of Synodontis spp. Whilst nuclear data were inconclusive, mitochondrial sequences suggested that both morphotypes and intermediate forms are conspecific. The results imply probable synonymy of S. frontosus with S. schall. Conversely, a strong biogeographical signal was revealed among widely distributed and supposedly conspecific S. schall-like catfish of the Nilo-Sudanian ichthyological province. Synodontis schall sensu stricto (=Eastern clade), as defined by type locality in the Nile, is apparently restricted to the eastern part of the Nilo-Sudanian ichthyological province (e.g. Nile, Turkana, Chad). Synodontis schall Western clade (Senegambia, Niger, Chad) most probably represents a cryptic taxon, unrecognized thus far due to the absence of distinctive morphological differences.

Erratum v

PubMed

Zobrazit více v PubMed

Gill BA, et al. Cryptic species diversity reveals biogeographic support for the ‘mountain passes are higher in the tropics’ hypothesis. Proc. R. Soc. B Biol. Sci. 2016;283:20160553. PubMed PMC

Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. 2004;101:14812–14817. PubMed PMC

Jörger KM, Schrödl M. How to describe a cryptic species? Practical challenges of molecular taxonomy. Front. Zool. 2013;10:59. PubMed PMC

Cooke GM, Chao NL, Beheregaray LB. Divergent natural selection with gene flow along major environmental gradients in Amazonia: insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus. Mol. Ecol. 2012;21:2410–27. PubMed

Piggott MP, Chao NL, Beheregaray LB. Three fishes in one: Cryptic species in an Amazonian floodplain forest specialist. Biol. J. Linn. Soc. 2011;102:391–403.

Souza CR, de Mello Affonso PRA, de Araújo Bitencourt J, Sampaio I, Carneiro PLS. Species validation and cryptic diversity in the Geophagus brasiliensis Quoy & Gaimard, 1824 complex (Teleostei, Cichlidae) from Brazilian coastal basins as revealed by DNA analyses. Hydrobiologia. 2018;809:309–321.

Katongo C, Koblmüller S, Duftner N, Makasa L, Sturmbauer C. Phylogeography and speciation in the Pseudocrenilabrus philander species complex in Zambian Rivers. Hydrobiologia. 2005;542:221–233.

Day JJ, et al. Multiple independent colonizations into the Congo Basin during the continental radiation of African Mastacembelus spiny eels. J. Biogeogr. 2017;44:2308–2318.

Martin AP, Bermingham E. Regional endemism and cryptic species revealed by molecular and morphological analysis of a widespread species of Neotropical catfish. R. Soc. 2009;267:1135–1141. PubMed PMC

Souza-Shibatta L, et al. Cryptic species of the genus Pimelodella (siluriformes: Heptapteridae) from the Miranda river, Paraguay River basin, Pantanal of Mato Grosso do Sul, Central Brazil. Neotrop. Ichthyol. 2013;11:101–109.

Prizon, A. C. et al. Hidden diversity in the populations of the armored catfish Ancistrus Kner, 1854 (Loricariidae, Hypostominae) from the Paraná River basin revealed by molecular and cytogenetic data. Front. Genet. 8 (2017). PubMed PMC

Wright JJ, Bailey RM. Systematic revision of the formerly monotypic genus Tanganikallabes (Siluriformes: Clariidae) Zool. J. Linn. Soc. 2012;165:121–142.

Barasa JE, et al. Genetic diversity and population structure of the African catfish, Clarias gariepinus (Burchell, 1822) in Kenya: implication for conservation and aquaculture. Belgian J. Zool. 2017;147:105–127.

Schmidt RC, Bart HL, Pezold F. High levels of endemism in suckermouth catfishes (Mochokidae: Chiloglanis) from the Upper Guinean forests of West Africa. Mol. Phylogenet. Evol. 2016;100:199–205. PubMed

Schmidt RC, Bart HL, Nyingi DW, Gichuki NN. Phylogeny of suckermouth catfishes (Mochokidae: Chiloglanis) from Kenya: The utility of Growth Hormone introns in species level phylogenies. Mol. Phylogenet. Evol. 2014;79:415–421. PubMed

Morris J, et al. High levels of genetic structure and striking phenotypic variability in a sexually dimorphic suckermouth catfish from the African Highveld. Biol. J. Linn. Soc. 2016;117:528–546.

Musschoot T, Lalèyè P. Designation of a neotype for Synodontis schall (Bloch and Schneider, 1801) and description of two new species of Synodontis (Siluriformes: Mochokidae) J. Nat. Hist. 2008;42:1303–1331.

Poll M. Révision des Synodontis africains (famille Mochokidae) Ann. – Musée R. l’Afrique Cent. Zool. 1971;191:1–497.

Lévêque C, Paugy D, Teugels GG. Annotated check-list of the freshwater fisltes of the Nilo-sudan river basins in Africa. Changes. 1991;24:131–154.

Bailey, R. G. Guide to the fishes of the River Nile in the Republic of the Sudan. J. Nat. Hist. 10.1080/00222939400770501(1994).

Paugy, D., Roberts, T. R. & Mochokidae, P. In C. Lévêque, D. Paugy and G.G. Teugels (eds.) Faune des poissons d’eaux douce et saumâtres de l’Afrique de l’Ouest, Tome 2. Coll. 195–268 (Faune et Flore tropicales 40. Musée Royal de l’Afrique Centrale, Tervuren, Belgique, Museum National d’Histoire Naturalle, Paris, France and Institut de Recherche pour le Développement, Paris, France. 815 p., 2003).

Hopson, A. Lake Turkana; A Report on the Finding of the Lake Turkana Project 1972–1975, Vols. 1–6. (Overseas Development Administration, London, 1982).

Jirsová D, Štefka J, Jirků M. Discordant population histories of host and its parasite: A role for ecological permeability of extreme environment? PLoS One. 2017;12:1–25. PubMed PMC

Eschmeyer, W. N., Fricke, R. & van der Laan, R. Catalog of fishes: genera, species, references, (http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Electronic version accessed 22/07/2017 (2017).

Froese, R. & Pauly, D. Fishbase. World Wide Web electronic publication, www.fishbase.org, version (02/2017). (2017). Available at, www.fishbase.org version (02/2017).

Koblmüller S, Sturmbauer C, Verheyen E, Meyer A, Salzburger W. Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: Synodontis) BMC Evol. Biol. 2006;6:49. PubMed PMC

Pinton A, Agnèse JF, Paugy D, Otero O. A large-scale phylogeny of Synodontis (Mochokidae, Siluriformes) reveals the influence of geological events on continental diversity during the Cenozoic. Mol. Phylogenet. Evol. 2013;66:1027–40. PubMed

Day JJ, et al. Continental diversification of an African catfish radiation (Mochokidae: Synodontis) Syst. Biol. 2013;62:351–365. PubMed

Sands, D. D. Catfishes of the World. Vol. 2: Mochokidae. (Dunure Enterprises, Dunure, Scotland, 1983).

Day JJ, Wilkinson M. On the origin of the Synodontis catfish species flock from Lake Tanganyika. Biol. Lett. 2006;2:548–552. PubMed PMC

Day JJ, Bills R, Friel JP. Lacustrine radiations in African Synodontis catfish. J. Evol. Biol. 2009;22:805–17. PubMed

Mohamed EHA. Characterization of two Synodontis (Siluriformes: Mochokidae) catfish species in the White Nile and Lake Nubia. Environ. Biol. Fishes. 2010;88:17–23.

Luff, R. M. & Bailey, G. The Aquatic Basis of Ancient Civilisaticlns:the case of Synodontis schal2 and the Nile Valley. in Human Ecodynamics. Symposia of the Association for Environmental Archaeology (eds. Charles, R. & Winder, N.) 100–113 (Oxbow Books, 2000).

El-Kasheif MA, Authman MMN, Ibrahim SA. Environmental studies on Synodontis schall (Bloch and Schneider, 1801) (Pisces: Siluriformes: Mochokidae) in The River Nile at Gizza Sector, Egypt: biological aspects and population dynamics. J. Fish. Aquat. Sci. 2012;7:104–133.

Gownaris NJ, Pikitch EK, Ojwang WO, Michener R, Kaufman L. Predicting species’ vulnerability in a massively perturbed system: The fishes of Lake Turkana, Kenya. PLoS One. 2015;10:1–24. PubMed PMC

Sambrook, J. & Russell, D. W. Molecular Cloning: A Laboratory Manual. Cold Spring Harb. Lab. Press. Cold Spring Harb. NY 999 (2001).

Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN. Universal primer cocktails for fish DNA barcoding. Mol. Ecol. Notes. 2007;7:544–548.

Sullivan JP, Lundberg JG, Hardman M. A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences. Mol. Phylogenet. Evol. 2006;41:636–62. PubMed

Werle E, Schneider C, Renner M, Völker M, Fiehn W. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res. 1994;22:4354–4355. PubMed PMC

Kearse M, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. PubMed PMC

Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066. PubMed PMC

Posada D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 2008;25:1253–1256. PubMed

Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science (80-.). 2001;294:2310–2314. PubMed

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

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003;52:696–704. PubMed

Rambaut, A., Drummond, A., Xie, D., Baele, G. & Suchard, M. Tracer v1.7, Available from, http://beast.community/tracer (2018). PubMed PMC

Leigh JW, Bryant D. Popart: Full-Feature Software for Haplotype Network Construction. Methods Ecol. Evol. 2015;6:1110–1116.

Clement M, Posada D, Crandall Ka. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 2000;9:1657–9. PubMed

Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. PubMed

Tobe SS, Kitchener A, Linacre A. Cytochrome b or cytochrome c oxidase subunit I for mammalian species identification-An answer to the debate. Forensic Sci. Int. Genet. Suppl. Ser. 2009;2:306–307.

Meyer BS, Matschiner M, Salzburger W. Disentangling incomplete lineage sorting and introgression to refine species-tree estimates for Lake Tanganyika Cichlid fishes. Syst. Biol. 2017;66:531–550. PubMed

Koblmüller S, et al. Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus. Hydrobiologia. 2017;791:35–50.

Koblmüller S, et al. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika - The result of repeated introgressive hybridization. BMC Evol. Biol. 2007;7:1–13. PubMed PMC

Harrison HB, et al. Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish. Mol. Ecol. 2017;26:5692–5704. PubMed

Bradley RD, Baker RJ. A test of the Genetic Species Concept: cytochrome-b sequences and mammals. J. Mammal. 2001;82:960–973. PubMed PMC

Goodier, S. A. M., Cotterill, F. P. D., O’Ryan, C., Skelton, P. H. & de Wit, M. J. Cryptic diversity of African tigerfish (genus Hydrocynus) reveals palaeogeographic signatures of linked Neogene geotectonic events. PLoS One6 (2011). PubMed PMC

Paugy, D., Zaiss, R. & Troubat, J. J. ‘Faunafri’. World Wide Web electronic publication, http://www.poissons-afrique.ird.fr/faunafri/, version (09/2017) (2008).

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...