Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-02-08
Page range: 367–376
Abstract views: 70
PDF downloaded: 1

A preliminary assessment of genetic divergence and distribution of Malagasy cave fish in the genus Typhleotris (Teleostei: Milyeringidae)

Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig
Zoologie et Biodiversité Animale, Université d'Antananarivo, PO. Box 906, 101 Antananarivo, Madagascar; and Centre National de Recherches sur l’Environnement (CNRE). PO. Box 1739, 101 Antananarivo, Madagascar.
University of Hamburg, Animal Ecology and Conservation, Martin-Luther-King Platz 3, 20146 Hamburg, Germany
Pisces Madagascar Typhleotris madagascariensis Typhleotris mararybe Typhleotris pauliani distribution DNA barcoding

Abstract

The genus Typhleotris contains three poorly known blind fish species, inhabiting aquifers in the limestone plateau of south-western Madagascar. Until recently these species were known from only few localities, and their pattern of genetic differentiation remains poorly studied. In this study we analyse 122 Typhleotris tissue samples collected from 12 localities, spanning the entire known range of the genus, and use DNA sequences to assign these samples to the three species known. The phylogeny based on the mitochondrial marker cox1 revealed three main clades corresponding to the three species: Typhleotris madagascariensis, T. mararybe and T. pauliani, differing by uncorrected pairwise sequence divergences of 6.3-9.8%. The distribution ranges of the three species overlapped widely: T. mararybe was collected only in a southern group of localities, T. madagascariensis was found in both the southern and the central group of localities, and T. pauliani occurred from the northernmost site to the southern group of localities; yet the three species did not share haplotypes in two nuclear genes, except for three individuals that we hypothesize are hybrids of T. pauliani with T. madagascariensis and T. mararybe. This pattern of concordant mitochondrial and nuclear divergence despite sympatry strongly supports the status of all three taxa as separate species. Phylogeographic structure was obvious in T. madagascariensis, with two separate shallow mitochondrial clades occupying (1) the central vs. (2) the southern group of populations, and in T. pauliani, with separate mitochondrial clades for (1) the northern vs. (2) the central/southern populations. The widespread occurrence of these three cave fish species suggests that the aquifers in south-western Madagascar have at least in the past allowed episodic dispersal and gene flow of subterraneous organisms, whereas the phylogeographic pattern of T. madagascariensis and T. pauliani provides evidence for isolation and loss of connectivity in the more recent past.

 

References

  1. Arnoult, J. (1959) Une nouvelle espèce de poisson aveugle de Madagascar: Typhleotris pauliani n. sp. Mémoires de l’Institut Scientifique de Madagascar, Série A, Biologie Animale, 13, 133–138.

    Banister, K.E. (1994) Glossogobius ankaranensis, a new species of blind cave goby from Madagascar (Pisces: Gobioidei: Gobiidae). Aqua: Journal of Ichthyology and Aquatic Biology, 1, 25–28.

    Benstead, J.P., DeRham, P.H., Gattolliat, J.-L., Gibbon, F.M., Loiselle, P.V., Sartori, M., Sparks, J.S. & Stiassny, M.L.J. (2003) Conserving Madagascar's freshwater biodiversity. Bioscience, 53, 1101–1111.
    https://doi.org/10.1641/0006-3568(2003)053[1101:CMFB]2.0.CO;2

    Berti, R. & Messana, G. (2010) Subterranean fishes of Africa. In: Trajano, E., Bichuette, M.E. & Kapoor, B.G. (Eds.), Biology of Subterranean Fishes. Science Publishers and CRC Press, New Hampshire, pp. 357–395.
    https://doi.org/10.1201/EBK1578086702-c10

    Chakrabarty, P., Davis, M.P. & Sparks, J.S. (2012) The first record of a trans-oceanic sister-group relationship between obligate vertebrate troglobites. PLoS One, 7, e44083.
    https://doi.org/10.1371/journal.pone.0044083

    Che, J., Chen, H.M., Jin, J.Q., Joang, K., Yuan, Z.Y., Murphy, R.W. & Zhang, Y.P. (2012) Universal COI primers for DNA barcoding amphibians. Molecular Ecology Resources, 12, 247–258.
    https://doi.org/10.1111/j.1755-0998.2011.03090.x

    Crottini, A., Madsen, O., Poux, C., Strauß, A., Vieites, D.R. & Vences, M. (2012) Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K–T boundary in Madagascar. Proceedings of the National Academy of Sciences of the U.S.A., 109, 5358–5363.

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) ModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
    https://doi.org/10.1038/nmeth.2109

    David, C. & Culver, T.P. (2009) The Biology of Caves and Other Subterranean Habitats. Oxford University Press, Oxford, 39 pp.

    de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
    https://doi.org/10.1080/10635150701701083

    Dworak, L. (2014) Hydrogeological survey at the SuLaMa project site - SW Madagascar. Unpublished thesis, Institute of Geology, Mineralogy and Geophysics, Ruhr-University, Bochum, 75 pp.

    Dworak, L., Rasoloariniaina, J.R., Raminosoa, N. & Englert, A. (2015) Hydrogéologie dans le sud-ouest de Madagascar. In : Kobbe, S., Verjans, J., Nopper, J., Riemann, J.C., Prill, L., Andrianasolo, T., Rakotondranary, J., Fraust, D., Ratsimbarison, R. & Kübler, D. (Eds.), Recherche participative pour le soutien de la gestion durable des terres du Plateau Mahafaly, dans le sud-ouest de Madagascar (SuLaMa) - Conclusion préliminaire. Université de Hambourg, Hambourg, pp. 38–44. Available from: http://www.sulama.de (Accessed 8 Feb. 2018)

    Felice, V., Visconti, M.A. & Trajano, M. (2008) Mechanisms of pigmentation loss in subterranean fishes. Neotropical Ichthyology, 6, 657–662.
    https://doi.org/10.1590/S1679-62252008000400015

    FishBase team RMCA & Sparks, J.S. (2016a) Typhleotris madagascariensis. The IUCN Red List of Threatened Species 2016: e.T22595A58303484.
    https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22595A58303484.en

    FishBase team RMCA & Sparks, J.S. (2016b) Typhleotris mararybe. The IUCN Red List of Threatened Species 2016: e.T57499221A58341136.
    https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T57499221A58341136.en

    FishBase team RMCA & Sparks, J.S. (2016c) Typhleotris pauliani. The IUCN Red List of Threatened Species 2016: e.T22596A58303542.
    https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22596A58303542.en

    Guyot, L. (2002) Reconnaissance hydrogéologique pour l’alimentation en eau d’une plaine littorale en milieu semi-aride: Sud-Ouest de Madagascar. Unpublished thesis, Faculté des Sciences et Techniques. Université de Nantes, Nantes. [unkown pagination]

    Jeffery, W.R. (2009) Regressive evolution in Astyanax cavefish. Annual Reviews of Genetics, 43, 25–47.
    https://doi.org/10.1146/annurev-genet-102108-134216

    Kiener, A. (1964) De la présence de certaines populations ichtyologiques dans les eaux souterraines des formations karstiques de la côte ouest de Madagascar. Bulletin de Madagascar, 21,573–592.

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
    https://doi.org/10.1093/molbev/msw054

    Landi, M., Dimech, M., Arculeo, M., Biondo, G., Martins, R., Carneiro, M., Carvalho, G.R., Lo Brutto, S. & Costa, F. (2014) DNA barcoding for species assignment: the case of Mediterranean marine fishes. PLoS ONE, 9, e106135.
    https://doi.org/10.1371/journal.pone.0106135

    Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
    https://doi.org/10.1093/bioinformatics/btp187

    Meyer, C., Geller, J. & Paulay, G. (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution, 59, 113–125.
    https://doi.org/10.1111/j.0014-3820.2005.tb00899.x

    Near, T.J., Eytan, R.I., Dornburg, A., Kuhn, K.L., Moore, J.A., Davis, M.P., Wainwright, P.C., Friedman, M. & Smith, W.L. (2012) Resolution of ray-finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences of the U.S.A., 109, 13698–13703.

    Pabijan, M., Brown, J., Chan, L.M., Rakotondravony, H., Raselimanana, A.P., Yoder, A.D., Glaw, F. & Vences, M. (2015) Phylogeography of the arid-adapted Malagasy bullfrog, Laliostoma labrosum, influenced by past connectivity and habitat stability. Molecular Phylogenetics and Evolution, 92, 11–24.
    https://doi.org/10.1016/j.ympev.2015.05.018

    Padial, J.M., Miralles, A., de la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16.
    https://doi.org/10.1186/1742-9994-7-16

    Pereiram, L.H.G., Hanner, R., Foresti, F. & Oliveira, C. (2013) Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genetics, 14, 20.

    Perl, R.G.B., Nagy, Z.T., Sonet, G., Glaw, F., Wollenberg, K.C. & Vences, M. (2014) DNA barcoding Madagascar’s amphibian fauna. Amphibia-Reptilia, 35, 197–206.
    https://doi.org/10.1163/15685381-00002942

    Petit, G. (1933) Un poisson cavernicole aveugle des eaux douces de Madagascar: Typhleotris madagascariensis gen. et sp. nov. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, 197, 347–348.

    Poulson, T.L. (2010) Cavefish: Retrospective and prospective. In: Trajano, E., Bichuette, M.E. & Kapoor, B.G. (Eds.), Biology of Subterranean Fishes. Science Publishers and CRC Press, New Hamsphire, pp. 1–39.
    https://doi.org/10.1201/EBK1578086702-c1

    Rabemananjara, F.C.E., Chiari, Y., Ravoahangimalala Ramilijaona, O. & Vences, M. (2007) Evidence for recent gene flow between north-eastern and south-eastern Madagascar from a phylogeography of the Mantella cowani group. Frontiers in Zoology, 4 (Article 1). [published online]

    Rasoloariniaina, J.R., Ganzhorn, J., Riemann, J.C. & Raminosoa, N. (2016) Water quality and biotic interaction of two cavefish species: Typhleotris madagascariensis (Petit 1933) and Typhleotris mararybe (Sparks & Chakrabarty 2012), in the Mahafaly Plateau groundwater system, Madagascar. Subterranean Biology, 18, 1–16.
    https://doi.org/10.3897/subtbiol.18.8321

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
    https://doi.org/10.1093/sysbio/sys029

    Rosenberger, A.L., Godfrey, L.R., Muldoon, K.M., Gunnell, G.F., Andriamialison, H., Ranivoharimanana, L., Ranaivoarisoa, J.F., Rasoamiaramanana, A.H., Randrianasy, J. & Amador, F.E. (2015) Giant subfossil lemur graveyard discovered, submerged, in Madagascar. Journal of Human Evolution, 81, 83–87.
    https://doi.org/10.1016/j.jhevol.2015.01.004

    Salzburger, W., Ewing, G.B. & Von Haeseler, A. (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology, 20, 1952–1963.
    https://doi.org/10.1111/j.1365-294X.2011.05066.x

    Shen, X.X., Liang, D. & Zhang, P. (2012) The development of three long universal nuclear protein-coding locus markers and their application to osteichthyan phylogenetics with nested PCR. PLoS ONE, 7, e39256.
    https://doi.org/10.1371/journal.pone.0039256

    Sparks, J.S. & Chakrabarty, P. (2012) Revision of the endemic Malagasy cavefish genus Typhleotris (Teleostei: Gobiiformes: Milyeringidae), with discussion of its phylogenetic placement and description of a new species. American Museum Novitates, 3764, 1–28.
    https://doi.org/10.1206/3764.2

    Sparks, J.S. & Stiassny, M.L.J. (2003) Introduction to the freshwater fishes. In: Goodman, S.M. & Benstead, J.P. (Eds.), The Natural History of Madagascar. The University of Chicago Press, Chicago/London, pp. 849–863.

    Stephens, M., Smith, N.J. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989.
    https://doi.org/10.1086/319501

    Sugimoto, M. (2002) Morphological color changes in fish: regulation of pigment cell density and morphology. Microscopy Research and Technique, 58, 496–503.
    https://doi.org/10.1002/jemt.10168

    Vences, M., Wollenberg, K.C., Vieites, D.R. & Lees, D.C. (2009) Madagascar as a model region of species diversification. Trends in Ecology and Evolution, 24, 456–465.
    https://doi.org/10.1016/j.tree.2009.03.011

    Vuataz, L., Sartori, M., Gattolliat, J.L. & Monaghan, M.T. (2013) Endemism and diversification in freshwater insects of Madagascar revealed by coalescent and phylogenetic analysis of museum and field collections. Molecular Phylogenetics and Evolution, 66, 979–991.
    https://doi.org/10.1016/j.ympev.2012.12.003

    Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D.N. (2005) DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society London B, 360, 1847–1857.
    https://doi.org/10.1098/rstb.2005.1716

    Wilmé, L., Goodman, S.M. & Ganzhorn, J.U. (2006) Biogeographic evolution of Madagascar's microendemic biota. Science, 312, 1063–1065.
    https://doi.org/10.1126/science.1122806