Abstract
The subgenus Brygoomantis in the Madagascar-endemic genus Mantidactylus contains 12 nominal species but is in urgent need of taxonomic revision as many additional, genetically divergent but undescribed candidate species have been identified. We here take a first step towards a better resolution of this group by describing a new species, Mantidactylus schulzi sp. nov., occurring at the Tsaratanana and Manongarivo Massifs, differentiated in genetic, bioacoustic and sometimes morphological characters from its closest relatives. We show that upon detailed study, most species in Brygoomantis can be delimited by concordant differentiation of mitochondrial and nuclear DNA, and by bioacoustic and morphological differences. We flag this group of morphologically similar frogs as a test case where molecular data on historical type specimens by ancient DNA methods might be needed to reach a satisfying clarification of taxonomy and nomenclature. However, the status of the new species M. schulzi is not in doubt as it is morphologically distinct from most historical type specimens, and microendemic to a region in northern Madagascar from where no earlier names exist.
References
AmphibiaWeb (2018) Information on amphibian biology and conservation. AmphibiaWeb, Berkeley, California. Available from: http://amphibiaweb.org/ (accessed 10 August 2018).
Andreone, F., Glaw, F., Mattioli, F., Jesu, R., Schimmenti, G., Randrianirina, J.E. & Vences, M. (2009) The peculiar herpetofauna of some Tsaratanana rainforests and its affinities with Manongarivo and other massifs and forests of northern Madagascar. Italian Journal of Zoology, 76, 92–110.
https://doi.org/10.1080/11250000802088603Avise, J.C. & Ball, R.M. (1990) Principles of genealogical concordance in species concepts and biological taxonomy. In: Futuyma, D. & Antonovics, J. (Eds.), Oxford surveys in evolutionary biology. Oxford Univ. Press, Oxford, pp. 45– 67.
Avise, J. & Wollenberg, K. (1997) Phylogenetics and the origin of species. Proceedings of the National Academy of Sciences of the United States of America, 94, 7748–7755.
https://doi.org/10.1073/pnas.94.15.7748Blommers-Schlösser, R.M.A. (1979) Biosystematics of the Malagasy frogs. I. Mantellinae (Ranidae). Beaufortia, 352, 1–77.
Blommers-Schlösser, R.M.A. & Blanc, C.P. (1991) Amphibiens (première partie). Faune de Madagascar, 75, 1–379.
Blommers-Schlösser, R.M.A. & Blanc, C.P. (1993) Amphibiens (deuxième partie). Faune de Madagascar, 75, 385–530.
Brown, J.L., Sillero, N., Glaw, F., Bora, P., Vieites, D.R. & Vences, M. (2016) Spatial biodiversity patterns of Madagascar's amphibians and reptiles. PLoS ONE, 11, e0144076.
https://doi.org/10.1371/journal.pone.0144076Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M. & Gemmell, N.J. (2007) Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE, 2, e1109.
https://doi.org/10.1371/journal.pone.0001109Frost, D.R. (2018) Amphibian Species of the World: an Online Reference. Version 6.0 (accessed 10 August 2018). American Museum of Natural History, New York, USA. Electronic Database accessible. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 29 August 2018)
Glaw, F., Köhler, J., De la Riva, I., Vieites, D.R. & Vences, M. (2010) Integrative taxonomy of Malagasy treefrogs: combination of molecular genetics, bioacoustics and comparative morphology reveals twelve additional species of Boophis. Zootaxa, 2383, 1–82.
Glaw, F. & Vences, M. (1994) A Fieldguide to the Amphibians and Reptiles of Madagascar. Second Edition, including Mammals and Freshwater Fish. Vences & Glaw Verlag, Cologne, 480 pp., 48 colour pls.
Glaw, F. & Vences, M. (1999) Resurrection and redescription of Mantidactylus tricinctus (Guibé, 1947) from eastern Madagascar (Anura: Ranidae: Mantellinae). Journal of Herpetology, 33, 639–647.
https://doi.org/10.2307/1565581Glaw, F. & Vences, M. (2004) A preliminary review of cryptic diversity in frogs of the subgenus Ochthomantis based on mtDNA sequence data and morphology (Anura, Mantellidae, Mantidactylus). Spixiana, 27, 83–91.
Glaw, F. & Vences, M. (2006) Phylogeny and genus-level classification of mantellid frogs (Amphibia, Anura). Organisms Diversity & Evolution, 6, 236–253.
https://doi.org/10.1016/j.ode.2005.12.001Glaw, F. & Vences, M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar. 3rd Edition. Vences & Glaw Verlag, Cologne, 496 pp.
Glaw, F., Vences, M. & Gossmann, V. (2000) A new species of Mantidactylus (subgenus Guibemantis) from Madagascar, with a comparative survey of internal femoral gland structure in the genus (Amphibia: Ranidae: Mantellinae). Journal of Natural History, 34, 1135–1154.
https://doi.org/10.1080/00222930050020140Grosjean, S., Strauß, A., Glos, J., Randrianiaina, R.-D., Ohler, A. & Vences, M. (2011) Morphological and ecological uniformity in the funnel-mouthed tadpoles of Malagasy litter frogs, subgenus Chonomantis. Zoological Journal of the Linnean Society, 162, 149–183.
https://doi.org/10.1111/j.1096-3642.2010.00667.xHykin, S.M., Bi, K. & McGuire, J.A. (2015) Fixing formalin: a method to recover genomic-scale DNA sequence data from formalin-fixed museum specimens using high-throughput sequencing. PLoS One, 10, e0141579.
https://doi.org/10.1371/journal.pone.0141579Junk, A., Wenzel, S., Vences, M. & Nowack, C. (2014) Deviant anatomy of the olfactory system of the Malagasy frog Mantidactylus betsileanus (Anura: Mantellidae). Zoologischer Anzeiger, 253, 338–344.
https://doi.org/10.1016/j.jcz.2013.11.004Knoll, A., Köhler, J., Glaw, F., Teschke, M. & Vences, M. (2007) Larval morphology in four species of Madagascan frogs of the subgenus Brygoomantis (Mantellidae: Mantidactylus). Zootaxa, 1616, 49–59.
Köhler, J., Jansen, M., Rodríguez, A., Kok, P.J.R., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rödel, M.-O. & Vences, M. (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa, 4251 (1), 1–124.
https://doi.org/10.11646/zootaxa.4251.1.1Kremen, C., Cameron, A., Moilanen, A., Phillips, S.J., Thomas, C.D., Beentje, H., Dransfield, J., Fisher, B.L., Glaw, F., Good, T.C., Harper, G.J., Hijmans, R.J., Lees, D.C., Louis Jr., E., Nussbaum, R.A., Raxworthy, C.J., Razafimpahanana, A., Schatz, G.E., Vences, M., Vieites, D.R. & Zjhra, M.L. (2008) Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science, 320, 222–226.
https://doi.org/10.1126/science.1155193
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.
https://doi.org/10.1093/molbev/msw054
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/btp187McGuire, J.A., Cotoras, D.D., O'Connell, B., Lawalata, S.Z.S., Wang-Claypool, C.Y., Stubbs, A., Huang, X., Wogan, G.O.U., Hykin, S.M., Reilly, S.B., Bi, K., Riyanto, A., Arida, E., Smith, L.L., Milne, H., Streicher, J.W. & Iskandar, D.T. (2018) Squeezing water from a stone: high-throughput sequencing from a 145-year old holotype resolves (barely) a cryptic species problem in flying lizards. PeerJ, 6, e4470.
Mercurio, V. & Andreone, F. (2007) Two new canyon-dwelling frogs from the arid sandstone Isalo Massif, central-southern Madagascar (Mantellidae, Mantellinae). Zootaxa, 1574, 31–47.
Nowack, C., Peram, P.S., Wenzel, S., Rakotoarison, A., Glaw, F., Poth, D., Schulz, S. & Vences, M. (2017) Volatile compound secretion coincides with modifications of the olfactory organ in mantellid frogs. Journal of Zoology, 303, 72–81.
https://doi.org/10.1111/jzo.12467Nowack, C. & Vences, M. (2016) Ontogenetic development of the derived olfactory system of the mantellid frog Mantidactylus betsileanus. Anatomical Record, 299, 943–950.
https://doi.org/10.1002/ar.23351Padial, J. M., Miralles, A., de la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, article 16.
https://doi.org/10.1186/1742-9994-7-16Peram, P.S., Vences, M. & Schulz, S. (2017) A synthetic dodecanolide library for the identification of putative semiochemicals emitted by mantellid frogs. Organic & Biomolecular Chemistry, 15, 6967–6977.
https://doi.org/10.1039/C7OB00849JPerl, 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/10.1163/15685381-00002942Poth, D., Peram, P.S., Vences, M. & Schulz, S. (2013) Macrolides and alcohols as scent gland constituents of the Madagascan frog Mantidactylus femoralis and their intraspecific diversity. Journal of Natural Products, 76, 1548–1558.
https://doi.org/10.1021/np400131qPoth, D., Wollenberg, K.C., Vences, M. & Schulz, S. (2012) Volatile amphibian pheromones: macrolides of mantellid frogs from Madagascar. Angewandte Chemie International Edition, 51, 2187–2190.
https://doi.org/10.1002/anie.201106592de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation Oxford University Press, New York, pp. 57–75.
Rakotoarison, A, Scherz, M.D., Glaw, F., Köhler, J., Andreone, F., Franzen, M., Glos, J., Hawlitschek, O., Jono, T., Mori, A., Ndriantsoa, S.H., Raminosa, N.R., Riemann, J.C., Rödel, M.-O., Rosa, G.M., Vieites, D.R., Crottini, A. & Vences, M. (2017) Describing the smaller majority: integrative taxonomy reveals twenty-six new species of tiny microhylid frogs (genus Stumpffia) from Madagascar. Vertebrate Zoology, 67, 271–398.
Randrianiaina, R.D., Strauß, A., Glos, J., Glaw, F. & Vences, M. (2011) Diversity, external morphology and ‘reverse taxonomy’ in the specialized tadpoles of Malagasy river bank frogs of the subgenus Ochthomantis (genus Mantidactylus). Contributions to Zoology, 80, 17–65.
Rosa, G.M., Andreone, F., Crottini, A., Hauswaldt, J.S., Noël, J., Rabibisoa, N.H., Randriambahiniarime, M.O., Rebelo, R. & Raxworthy, C.J. (2012) The amphibians of the relict Betampona low-elevation rainforest, eastern Madagascar: an application of the integrative taxonomy approach to biodiversity assessments. Biodiversity and Conservation, 21, 1531–1559.
https://doi.org/10.1007/s10531-012-0262-xRuane, S. & Austin, C.C. (2017) Phylogenomics using formalin-fixed and 100+ year-old intractable natural history specimens. Molecular Ecology Resources, 17, 1003–1008.
https://doi.org/10.1111/1755-0998.12655Salzburger, 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.xScherz, M.D., Hawlitschek, O., Andreone, F., Rakotoarison, A., Vences, M. & Glaw, F. (2017) A review of the taxonomy and osteology of the Rhombophryne serratopalpebrosa species group (Anura: Microhylidae) from Madagascar, with comments on the value of volume rendering of micro-CT data to taxonomists. Zootaxa, 4273 (3), 301–340.
https://doi.org/10.11646/zootaxa.4273.3.1Schmidt, H., Strauß, A., Glaw, F., Teschke, M. & Vences, M. (2009) Description of tadpoles of five frog species in the subgenus Brygoomantis from Madagascar (Mantellidae: Mantidactylus). Zootaxa, 1988, 48–60.
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/10.1086/319501Thomas, M., Raharivololoniaina, L., Glaw, F., Vences, M. & Vieites, D.R. (2005) Montane tadpoles in Madagascar: molecular identification and description of the larval stages of Mantidactylus elegans, Mantidactylus madecassus, and Boophis laurenti from the Andringitra Massif. Copeia, 2005, 174–183.
https://doi.org/10.1643/CH-03-293R2Vejarano, S., Thomas, M., Glaw, F. & Vences, M. (2006) Advertisement call and tadpole morphology of the clutch-guarding frog Mantidactylus argenteus from eastern Madagascar. African Zoology, 41, 164–169.
https://doi.org/10.1080/15627020.2006.11407351Vences, M., Gehara, M., Köhler, J. & Glaw, F. (2012) Description of a new Malagasy treefrog (Boophis) occurring syntopically with its sister species, and a plea for studies on non-allopatric speciation in tropical amphibians. Amphibia-Reptilia, 33, 503–520.
https://doi.org/10.1163/15685381-00002856Vences, M. & Glaw, F. (1999) Variation in Mantidactylus madecassus Millot & Guibé, 1950, a little known Malagasy frog, with resurrection of Mantidactylus pauliani Guibé, 1974. Herpetological Journal, 9, 101–110.
Vences, M. & Glaw, F. (2004) Revision of the subgenus Chonomantis (Anura: Mantellidae: Mantidactylus) from Madagascar, with description of two new species. Journal of Natural History, 38, 77–118.
https://doi.org/10.1080/0022293021000010331Vences, M., Glaw, F. & Márquez, R. (2006) The Calls of the Frogs of Madagascar. Alosa-Fonozoo, Barcelona, 44 pp., 3 Audio CDs, booklet.
Vences, M., Kosuch, J., Glaw, F., Böhme, W. & Veith, M. (2003) Molecular phylogeny of hyperoliid treefrogs: biogeographic origin of Malagasy and Seychellean taxa and re-analysis of familial paraphyly. Journal of Zoological Systematics and Evolutionary Research, 41, 205–215.
10.1046/j.1439-0469.2003.00205.xVieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the USA, 106, 8267–8272.
https://doi.org/10.1073/pnas.0810821106Wilmé, 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.1122806Wollenberg, K.C., Vieites, D.R., Glaw, F. & Vences, M. (2011) Speciation in little: the role of range and body size in the diversification of Malagasy mantellid frogs. BMC Evolutionary Biology, 11, 217.
https://doi.org/10.1186/1471-2148-11-217Wollenberg Valero, K.C., Garcia-Porta, J., Rodríguez, A., Arias, M., Shah, A., Randrianiaina, R.D., Brown, J.L., Glaw, F., Amat, F., Künzel, S., Metzler, D., Isokpehi, R.D. & Vences, M. (2017) Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nature Communications, 8, 15213.
https://doi.org/10.1038/ncomms15213