Abstract
The Malagasy frog Platypelis mavomavo from Ambolokopatrika in the North East of Madagascar was originally diagnosed based on its bright yellow venter, but only limited information on this species has become available after its initial description in 2003. Several Platypelis specimens with yellow ventral color have been erroneously assigned to this species due to a lack of DNA sequences from the P. mavomavo type series. On the other hand, the candidate species Platypelis sp. Ca10 from Andranomapanga in the Northern Central East of Madagascar with gray ventral color has been defined based on its genetic differentiation from other nominal Platypelis species. Here we study the genetic variation of P. mavomavo and P. sp. Ca10 based on mitochondrial (16S rRNA) and nuclear-encoded (RAG-1) genes, including a newly determined sequence from the P. mavomavo holotype, which was studied using a museomics approach. We find only limited genetic variation among the samples studied, and this variation is unlinked to ventral coloration but instead reflects geographic distribution. We, therefore, conclude that P. sp. Ca10 is a gray-colored variant of P. mavomavo, and that P. mavomavo is rather widespread in the North East and Northern Central East of Madagascar, with populations in areas bordering the North West (Ambohitantely) and Sambirano (Ampotsidy) geographic regions, and the yellow-bellied morph restricted to the North East (Makira, Ambolokopatrika). Due to the range extension of P. mavomavo, the conservation status of the species requires re-assessment.
References
- Andreone, F., Fenolio, D.B. & Walvoord, M.E. (2003) Two unknown arboreal frogs (genus Platypelis) described from the rainforests of northeastern Madagascar (Microhylidae: Cophylinae). Current Herpetology, 22, 91–100. https://doi.org/10.5358/hsj.22.91
- Andreone, F., Fenolio, D.B. & Walvoord, M.E. (2004) Erratum: “Two unknown arboreal frogs (genus Platypelis) described from the rainforests of northeastern Madagascar (Microhylidae: Cophylinae)”. Current Herpetology, 23, 85–86.
- Andreone, F., Vences, M., Vieites D.R., Glaw, F. & Meyer, A. (2005) Recurrent ecological adaptations revealed through a molecular analysis of the secretive cophyline frogs of Madagascar. Molecular Phylogenetics and Evolution, 34, 315–322. https://doi.org/10.1016/j.ympev.2004.10.013
- Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Single-locus and multilocus DNA fingerprint. In: Hoelzel, A.R. (Ed.), Molecular Genetic Analysis of Populations: A Practical Approach. IRL Press, Oxford, pp. 225–270.
- Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12, 373–377. https://doi.org/10.1111/2041-210X.13512
- Fulton, T.L. & Shapiro, B. (2019) Setting up an ancient DNA laboratory. Methods in Molecular Biology, 1963, 1–13. https://doi.org/10.1007/978-1-4939-9176-1_1
- Gansauge, M.-T., Gerber, T., Glocke, I., Korlević, P., Lippik, L., Nagel, S., Riehl, L.M., Schmidt, A. & Meyer, M. (2017) Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase. Nucleic Acids Research, 45, e79. https://doi.org/10.1093/nar/gkx033
- Glaw, F., Köhler, J., Crottini, A., Gehring, P.-S., Prötzel, D., Randriamanana, L., Andreone, F. & Vences M. (2021) An additional level of cryptic diversity: a new green-coloured Malagasy treefrog of the Boophis luteus species group. Salamandra, 57, 295–308.
- Glaw, F., Köhler, J. & Vences, M. (2012) A tiny new species of Platypelis from the Marojejy National Park in northeastern Madagascar (Amphibia: Microhylidae). European Journal of Taxonomy, 9, 1–9. https://doi.org/10.5852/ejt.2012.9
- Glaw, F., Scherz, M.D., Rakotoarison, A., Crottini, A., Raselimanana, A.P., Andreone, F., Köhler, J. & Vences, M. (2020) Genetic variability and partial integrative revision of Platypelis frogs (Microhylidae) with red flash marks from eastern Madagascar. Vertebrate Zoology, 70, 141–156.
- Glaw, F. & Vences, M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar. 3rd Edition. Vences & Glaw Verlags GbR, Cologne, 496 pp. [Third Edition.]
- IUCN (2022) The IUCN Red List of Threatened Species. Version 2022-2. IUCN, Gland and Cambridge. Available from: https://www.iucnredlist.org (accessed 28 February 2023)
- Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
- Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 3, 1870–1874. https://doi.org/10.1093/molbev/msw054
- Librado, P. & Rozas, J. (2009) DnaSP. Version 5. A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
- Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal, 1, 10–12. https://doi.org/10.14806/ej.17.1.200
- Mullin, K.E., Rakotomanga, M.G., Dawson J., Glaw, F., Rakotoarison, A., Orozco-terWengel, P. & Scherz, M.D. (2022) An unexpected new red-bellied Stumpffia (Microhylidae) from forest fragments in central Madagascar highlights remaining cryptic diversity. Zookeys, 1104, 1–28. https://doi.org/10.3897/zookeys.1104.82396
- Paijmans, J.L.A., Baleka, S., Henneberger, K., Taron, U.H., Trinks, A., Westbury, M.V. & Barlow, A. (2017) Sequencing single-stranded libraries on the Illumina NextSeq 500 platform. ArXiv, 2017, arXiv:1711.11004.
- Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool's guide to PCR, Version 2.0. Privately published, University of Hawaii.
- 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
- Rabearivony, J., Raselimanana, A.P., Andriamazava, M.A., Thorstrom, R. & de Roland, L.-A.R. (2010) A new locality for the endangered microhylid frog Scaphiophryne boribory from northern Madagascar and a rapid survey of other amphibians of the Bemanevika region. Herpetology Notes, 3, 105–109.
- Rakotoarison, A., Crottini, A., Müller, J., Rödel, M.-O., Glaw, F. & Vences, M. (2015) Revision and phylogeny of narrow-mouthed treefrogs (Cophyla) from northern Madagascar: integration of molecular, osteological, and bioacoustic data reveals three new species, Zootaxa, 3937 (1), 61–89. https://doi.org/10.11646/zootaxa.3937.1.3
- Rakotoarison, A., Glaw, F., Vieites, D.R., Raminosoa, N.R. & Vences, M. (2012) Taxonomy and natural history of arboreal microhylid frogs (Platypelis) from the Tsaratanana Massif in northern Madagascar, with description of a new species. Zootaxa, 3563 (1), 1–25. https://doi.org/10.11646/zootaxa3563.1.1
- Rakotoarison, A., Scherz, M.D., Bletz, M.C., Razafindraibe, J.H., Glaw, F. & Vences, M. (2019a) Description of the lucky Cophyla (Microhylidae, Cophylinae), a new arboreal frog from Marojejy National Park in north-eastern Madagascar. Zootaxa, 4651 (2), 271–288. https://doi.org/10.11646/zootaxa.4651.2.4
- Rakotoarison, A., Scherz, M.D., Bletz, M.C., Razafindraibe, J.H., Glaw, F. & Vences, M. (2019b) Diversity, elevational variation, and phylogenetic origin of stump-toed frogs (Microhylidae: Cophylinae: Stumpffia) on the Marojejy massif, northern Madagascar. Salamandra, 55, 115–123.
- Rakotoarison, A., Scherz, M.D., Glaw, F., Köhler, J., Andreone, F., Franzen, M., Glos, J., Hawlitschek, O., Jono, T., Mori, A., Ndriantsoa, S.H., Rasoamampionona Raminosoa, N., 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. https://doi.org/10.3897/vz.67.e31595
- Rakotoarison, A., Scherz, M.D., Köhler, J., Ratsoavina, F.M., Hawlitschek, O., Megson, S., Vences, M. & Glaw, F. (2020) Frogs of the genus Platypelis from the Sorata massif in northern Madagascar: description of a new species and reports of range extensions. Zoosystematics and Evolution, 96, 263–274. https://doi.org/10.3897/zse.96.47088
- Rohland, N., Siedel, H. & Hofreiter, M. (2004) Nondestructive DNA extraction method for mitochondrial DNA analyses of museum specimens. Biotechniques, 36, 814–821. https://doi.org/10.2144/04365ST05
- 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-x
- Rosa, G.M., Crottini, A., Noël, J., Rabibisoa, N., Raxworthy, C.J. & Andreone, F. (2014) A new phytotelmic species of Platypelis (Microhylidae: Cophylinae) from the Betampona Reserve, Eastern Madagascar. Salamandra, 50, 201–214.
- 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
- Scherz, M.D., Köhler, J., Vences, M. & Glaw, F. (2019) A new yellow-toed Platypelis species (Anura, Microhylidae, Cophylinae) from the Maroantsetra region, northeastern Madagascar. Evolutionary Systematics, 3, 75–83. https://doi.org/10.3897/evolsyst.3.33417
- Scherz, M.D., Vences, M., Rakotoarison, A., Andreone, F., Köhler, J., Glaw, F. & Crottini, A. (2016) Reconciling molecular phylogeny, morphological divergence and classification of Madagascan narrow-mouthed frogs (Amphibia: Microhylidae). Molecular Phylogenetics and Evolution, 100, 372–381. https://doi.org/10.1016/j.ympev.2016.04.019
- Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
- 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
- Straube, N., Lyra, M.L., Paijmans, J.L.A., Preick, M., Basler, N., Penner, J., Rödel, M.-O., Westbury, M.V., Haddad, C.F., Barlow, A. & Hofreiter, M. (2021) Successful application of ancient DNA extraction and library construction protocols to museum wet collection specimens. Molecular Ecology Resources, 21, 2299–2315. https://doi.org/10.1111/1755-0998.13433
- 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. https://doi.org/10.1046/j.1439-0469.2003.00205.x
- Vences, M., Miralles, A., Brouillet, S., Ducasse, J., Fedosov, A., Kharchev, V., Kostadinov, I., Kumari, S., Patmanidis, S., Scherz, M.D., Puillandre, N. & Renner S.S. (2021) iTaxoTools 0.1: Kickstarting a specimen-based software toolkit for taxonomists. Megataxa, 6 (2), 77–92. https://doi.org/10.11646/megataxa.6.2.1
- Vences, M., Patmanidis, S. Kharchev, V. & Renner, S.S. (2022) Concatenator, a user-friendly program to concatenate DNA sequences, implementing graphical user interfaces for MAFFT and FastTree. Bioinformatics Advances, 2, vbac050. https://doi.org/10.1093/bioadv/vbac050
- Vieites, 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 U.S.A., 106, 8267–8272. https://doi.org/10.1073/pnas.0810821106
- Wollenberg, K.C., Vieites, D.R., van der Meijden, A., Glaw, F., Cannatella, D.C. & Vences, M. (2008) Patterns of endemism and species richness in Malagasy cophyline frogs support a key role of mountainous areas for speciation. Evolution, 62, 1890–1907. https://doi.org/10.1111/j.1558-5646.2008.00420.x