Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-06-19
Page range: 97-115
Abstract views: 1287
PDF downloaded: 29

A new species of Pandanus-dwelling frog from northern Madagascar related to Guibemantis pulcher

Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
Museum of Natural Sciences and Department of Biological Sciences; Louisiana State University; Baton Rouge; LA 70803; USA
Zoologische Staatssammlung München (ZSM-SNSB); Münchhausenstr. 21; 81247 München; Germany
School for International Training; VN 41A Bis Ankazolava Ambohitsoa; Antananarivo 101; Madagascar
Mention Zoologie et Biodiversité Animale; Université d’Antananarivo; BP 906; Antananarivo 101; Madagascar; Association Vahatra; Lot V A 38 LBA Ter Ambohidempona Tsiadana; BP 3972; Antananarivo; 101; Madagascar
Natural History Museum of Denmark; University of Copenhagen; Universitetsparken 15; 2100; Copenhagen; Denmark
Amphibia Anura Mantellidae northern Madagascar phytotelmic anurans Guibemantis pulcher Guibemantis pulcherrimus sp. nov.

Abstract

Populations of phytotelmic frogs from northern Madagascar assigned to Guibemantis (Pandanusicola) pulcher are known to differ genetically from populations further south in the eastern rainforest belt of the island, but to date, their status has not been analyzed in depth. We combined molecular genetic data with an examination of color pattern to clarify the taxonomy of these frogs. DNA sequences of both mitochondrial and nuclear-encoded genes were consistently differentiated between the northern populations and those occurring further south. Uncorrected pairwise distance in the 16S rRNA gene was 3.7‒4.3% and thus at a level usually characterizing distinct frog species in Madagascar. Furthermore, the northern specimens were characterized by more and smaller purplish-brown spots on their green dorsal surface, and a less distinct brown patch on the flanks. Although fully conclusive evidence for the species status of the northern lineage from bioacoustic differences, sympatric occurrence or narrow hybrid zone is currently lacking, such species-level distinctness is currently the most likely hypothesis. We therefore name the northern populations as Guibemantis (Pandanusicola) pulcherrimus sp. nov. The new species is known from Makira (type locality) and Bemanevika, and specimens morphologically assignable to this taxon have also been recorded from Masoala, Marojejy and Anjanaharibe-Sud.

 

References

  1. Avise, 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 University Press, Oxford, pp. 45–67.
  2. Avise, J.C. & 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.94.15.7748 DOI: https://doi.org/10.1073/pnas.94.15.7748
  3. Bletz, M.C., Scherz, M.D., Rakotoarison, A., Lehtinen, R.M., Glaw, F. & Vences, M. (2018) Stumbling upon a new frog species of Guibemantis (Anura: Mantellidae) on the top of the Marojejy massif in northern Madagascar. Copeia, 106, 255–263. https://doi.org/10.1643/CH-17-655 DOI: https://doi.org/10.1643/CH-17-655
  4. Blommers-Schlösser, R.M.A (1979) Biosystematics of the Malagasy frogs. I. Mantellinae (Ranidae). Beaufortia, 29, 1–77.
  5. Blommers-Schlösser, R.M.A. & Blanc, C.P. (1991) Amphibiens (première partie). Faune de Madagascar, 75 (1), 1–379.
  6. Bossuyt, F. & Milinkovitch, M.C. (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences of the United States of America, 97, 6585–6590. https://doi.org/10.1073/pnas.97.12.6585 DOI: https://doi.org/10.1073/pnas.97.12.6585
  7. Boulenger, G.A. (1882) Catalogue of the Batrachia Salientia s. Ecaudata in the Collection of the British Museum. Taylor and Francis, London, UK. 2nd Edition.
  8. Boumans, L., Vieites, D.R., Glaw, F. & Vences, M. (2007) Geographical patterns of deep mitochondrial differentiation in widespread Malagasy reptiles. Molecular Phylogenetics and Evolution, 45, 822–839. https://doi.org/10.1016/j.ympev.2007.05.028 DOI: https://doi.org/10.1016/j.ympev.2007.05.028
  9. 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.0144076 DOI: https://doi.org/10.1371/journal.pone.0144076
  10. 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.
  11. de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms. Species and Speciation. Oxford University Press, Oxford, pp. 49–89.
  12. de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083 DOI: https://doi.org/10.1080/10635150701701083
  13. Dubois, A. (1992) Notes sur la classification des Ranidae (Amphibiens, Anoures). Bulletin Mensuel de la Société Linnéenne de Lyon, 61, 305–352. https://doi.org/10.3406/linly.1992.11011 DOI: https://doi.org/10.3406/linly.1992.11011
  14. Dufresnes, C., Brelsford, A., Jeffries, D.L., Mazepa, G., Suchan, T., Canestrelli, D., Nicieza, A., Fumagally, L., Dubey, S., Martinez-Solano, I., Litvinchuk, S.N., Vences, M., Perrin, N. & Crochet, P.-A. (2021) Master genes or mass of genes? A view on the genomic architecture of speciation from amphibian hybrid zones. Proceedings of the National Academy of Sciences of the United States of America, 118, e2103963118. https://doi.org/10.1073/pnas.2103963118 DOI: https://doi.org/10.1073/pnas.2103963118
  15. 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 DOI: https://doi.org/10.1111/2041-210X.13512
  16. Folmer, O.M., Black, Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biotechnology, 3, 294–299.
  17. Fouquet, 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.0001109 DOI: https://doi.org/10.1371/journal.pone.0001109
  18. Glaw, F. & Vences, M. (1994) A Fieldguide to the Amphibians and Reptiles of Madagascar. 2nd Edition. Vences and Glaw Verlag, Cologne, 448 pp.
  19. Glaw F. & Vences M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar. 3rd Edition. Vences and Glaw Verlag, Cologne, 496 pp.
  20. Hrbek, T. & Larson, A. (1999) The evolution of diapause in the killifish family Rivulidae (Atherinomorpha, Cyprinodontiformes): a molecular phylogenetic and biogeographic perspective. Evolution, 53, 1200–1216. https://doi.org/10.2307/2640823 DOI: https://doi.org/10.1111/j.1558-5646.1999.tb04533.x
  21. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285 DOI: https://doi.org/10.1038/nmeth.4285
  22. 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 DOI: https://doi.org/10.1093/molbev/mst010
  23. Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196–6200. https://doi.org/10.1073/pnas.86.16.6196 DOI: https://doi.org/10.1073/pnas.86.16.6196
  24. Koppetsch, T., Pabijan, M., Hutter, C.R., Köhler, J., Gehring, P.-S., Rakotoarison, A., Ratsoavina, F.M., Scherz, M.D., Vieites, D.R., Glaw, F. & Vences, M. (2023) An initial molecular resolution of the mantellid frogs of the Guibemantis liber complex reveals three new species from northern Madagascar. Vertebrate Zoology, 73, 397–432. https://doi.org/10.3897/vz.73.e94063 DOI: https://doi.org/10.3897/vz.73.e94063.suppl1
  25. 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 DOI: https://doi.org/10.1093/molbev/msw054
  26. Lehtinen, R.M. (2002) The use of screw pines (Pandanus spp.) by amphibians and reptiles in Madagascar. Herpetological Bulletin, 82, 20–25.
  27. Lehtinen, R.M. (2003) Parental care and reproduction in two species of Mantidactylus (Anura: Mantellidae). Journal of Herpetology, 37, 766–768. https://doi.org/10.1670/87-03N DOI: https://doi.org/10.1670/87-03N
  28. Lehtinen, R.M. (2004) Tests for competition, cannibalism, and priority effects in two phytotelm-dwelling tadpoles from Madagascar. Herpetologica, 60, 1–13. https://doi.org/10.1655/02-88 DOI: https://doi.org/10.1655/02-88
  29. Lehtinen, R.M. (2005) Competitive interactions and distributional dynamics in two Malagasy frogs. Journal of Tropical Ecology, 21, 569–576. https://doi.org/10.1017/S0266467405002580 DOI: https://doi.org/10.1017/S0266467405002580
  30. Lehtinen, R.M. (2009) The natural history of two plant-breeding frogs from Madagascar, Guibemantis bicalcaratus and G. punctatus (Anura: Mantellidae). Salamandra, 45, 39–49.
  31. Lehtinen, R.M. & Carfagno, G.L. (2011) Habitat selection, the included niche, and coexistence in plant‐specialist frogs from Madagascar. Biotropica, 43, 58–67. https://doi.org/10.1111/j.1744-7429.2010.00730.x DOI: https://doi.org/10.1111/j.1744-7429.2010.00730.x
  32. Lehtinen, R.M., Glaw, F., Andreone, F., Pabijan, M. & Vences, M. (2012) A new species of putatively pond breeding frog of the genus Guibemantis from Madagascar. Copeia, 2012, 648–662. https://doi.org/10.1643/CH-11-128 DOI: https://doi.org/10.1643/CH-11-128
  33. Lehtinen, R.M., Glaw, F., Vences, M., Rakotoarison, A. & Scherz, M.D. (2018) Two new Pandanus frogs (Guibemantis: Mantellidae: Anura) from northern Madagascar. European Journal of Taxonomy, 451, 1–20. https://doi.org/10.5852/ejt.2018.451 DOI: https://doi.org/10.5852/ejt.2018.451
  34. Lehtinen, R.M., Glaw, F. & Vences, M. (2011) Two new plant-breeding frog species (Anura: Mantellidae, Guibemantis) from southeastern Madagascar. Herpetological Journal, 21, 95–112.
  35. Lehtinen, R.M., Nussbaum, R.A., Richards, C.M., Cannatella, D.C. & Vences, M. (2007) Mitochondrial genes reveal cryptic diversity in plant-breeding frogs from Madagascar (Anura, Mantellidae, Guibemantis). Molecular Phylogenetics and Evolution, 44, 1121–1129. https://doi.org/10.1016/j.ympev.2007.05.020 DOI: https://doi.org/10.1016/j.ympev.2007.05.020
  36. Lehtinen, R.M., Scherz, M.D. & Vences, M. (2022) Mantellidae, Mantellinae: Guibemantis. In: Goodman, S.M. (Ed.), The New Natural History of Madagascar. Princeton University Press, Princeton, New Jersey, pp. 1374–1378. https://doi.org/10.2307/j.ctv2ks6tbb.192 DOI: https://doi.org/10.2307/j.ctv2ks6tbb.192
  37. 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 DOI: https://doi.org/10.1093/bioinformatics/btp187
  38. Millot, J. & Guibé, J. (1951) Batraciens malgaches a biotope vegetal. Mémoires de l’Institut Scientifique de Madagascar (A), 5 (1), 197–212.
  39. Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300 DOI: https://doi.org/10.1093/molbev/msu300
  40. 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 DOI: https://doi.org/10.1186/1742-9994-7-16
  41. 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, Honolulu, 45 pp.
  42. Rakotomalala, D. & Raselimanana, A. (2003) Les amphibiens et les reptiles des massifs de Marojejy, d’Anjanaharibe-Sud et du couloir forestier Betaolana. Recherches pour le Développement, Séries Sciences Biologiques, 19, 147–202.
  43. 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 DOI: https://doi.org/10.1111/j.1365-294X.2011.05066.x
  44. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675. https://doi.org/10.1038/nmeth.2089 DOI: https://doi.org/10.1038/nmeth.2089
  45. 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 DOI: https://doi.org/10.1371/journal.pone.0039256
  46. Speybroeck, J., Beukema, W., Dufresnes, C., Fritz, U., Jablonski, D., Lymberakis, P., Martínez-Solano, I., Razzetti, E., Vamberger, M., Vences, M., Vörös, J. & Crochet, P.A. (2020) Species list of the European herpetofauna—2020 update by the Taxonomic Committee of the Societas Europaea Herpetologica. Amphibia-Reptilia, 41, 139–189. https://doi.org/10.1163/15685381-bja10010 DOI: https://doi.org/10.1163/15685381-bja10010
  47. 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 DOI: https://doi.org/10.1093/bioinformatics/btu033
  48. 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 DOI: https://doi.org/10.1086/319501
  49. Vences, M., Glaw, F. & Marquez, R. (Eds.) (2006) The Calls of the Frogs of Madagascar. Alosa, Barcelona, 3 Audio CD’s, booklet 44 pp. [ISBN 84-609-8402-8]
  50. Vences, M., Hauswaldt, S. & Glaw, F. (2011) The advertisement call of Guibemantis pulcher, a phytotelmic frog from Madagascar. Herpetology Notes, 4, 377–379.
  51. Vences, M., Köhler, J., Andreone, F., Craul, A.-K., Crottini, A., du Preez, L., Preick, M., Rancilhac, L., Rödel, M.-O., Scherz, M.D., Streicher, J.W., Hofreiter, M. & Glaw, F. (2021) Target-enriched DNA sequencing clarifies the identity of name-bearing types of the Gephyromantis plicifer complex and reveals a new species of mantellid frog from Madagascar. Spixiana, 44, 175–202.
  52. 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 DOI: https://doi.org/10.1046/j.1439-0469.2003.00205.x
  53. 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 DOI: https://doi.org/10.1093/bioadv/vbac050
  54. Vences, M., Rakotoarison, A., Rakotondrazafy, A.M.A., Ratsoavina, F.M., Randrianiaina, R.D., Glaw, F., Lehtinen, R.M. & Raxworthy, C.J. (2013) Assessing the diversity of phytotelmic frogs along Madagascar’s east coast: Redefinition of Guibemantis bicalcaratus (Boettger, 1913) and revalidation of Guibemantis methueni (Angel, 1929). Vertebrate Zoology, 63, 193–205. https://doi.org/10.3897/vz.63.e31427 DOI: https://doi.org/10.3897/vz.63.e31427
  55. 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 Science of the United States of America, 106, 8267–8272. https://doi.org/10.1073/pnas.0810821106 DOI: https://doi.org/10.1073/pnas.0810821106