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Issue: Vol. 5446 No. 2: 30 Apr. 2024
Type: Article
Published: 2024-04-30
DOI: 10.11646/zootaxa.5446.2.3
Page range: 205-220
Abstract views: 54
PDF downloaded: 6

Molecular systematics of the subgenus Gephyromantis (Phylacomantis) with description of a new subspecies

Natural History Museum of Denmark; University of Copenhagen; Universitetsparken 15; 2100; Copenhagen Ø; Denmark
Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
The Peregrine Fund’s Project in Madagascar; B. P. 4113; Antananarivo 101; Madagascar
Mention Zoologie et Biodiversité Animale; Université d’Antananarivo; BP 906; Antananarivo 101; Madagascar
CIBIO; Centro de Investigação em Biodiversidade e Recursos Genéticos; InBIO Laboratório Associado; Campus de Vairão; Universidade do Porto; 4485-661 Vairão; Portugal; Departamento de Biologia; Faculdade de Ciências; Universidade do Porto; 4099-002 Porto; Portugal; BIOPOLIS Program in Genomics; Biodiversity and Land Planning; CIBIO; Campus de Vairão; 4485-661 Vairão; Portugal; BIOPOLIS Program in Genomics; Biodiversity and Land Planning; CIBIO; Campus de Vairão; 4485-661 Vairão; Portugal
Museo Regionale di Scienze Naturali; Via G. Giolitti; 36; 10123 Torino; Italy
Zoologische Staatssammlung München (ZSM-SNSB); Münchhausenstr. 21; 81247 München; Germany
Zoologisches Institut; Technische Universität Braunschweig; Mendelssohnstr. 4; 38106 Braunschweig; Germany
Amphibia Mantellidae subspecies G. corvus bakilana ssp. nov. Madagascar-Comoro Gephyromantis species richness biogeographic pattern humid forest fragments

Abstract

The mantellid subgenus Phylacomantis (genus Gephyromantis) currently contains four species of frogs distributed in the South (G. corvus, G. kintana), West (G. atsingy), North East, North, and Sambirano regions (G. pseudoasper) in Madagascar. We assess the molecular systematics of these amphibians based on extended sampling and analysis of multiple nuclear-encoded and mitochondrial genes. We confirm the delimitation of the four known species, which form monophyletic groups in a mitochondrial tree and separate phylogroups without haplotype sharing in haplotype networks of four nuclear markers. Newly included samples of G. pseudoasper from the North and North East regions confirm a comparatively low genetic variation of this species across its range, with pairwise genetic distance in the 16S gene not exceeding 1.4%. On the contrary, newly collected specimens from three sites in the North East and North West of the island strongly differed from all other Phylacomantis, with genetic distances exceeding 4.8% for the16S gene. Mitochondrial and nuclear markers strongly suggest them to be sister to G. corvus from the South. Due to haplotype sharing in two nuclear genes, absence of detectable morphological differences, and lack of data on bioacoustic differentiation, we describe these populations as a new subspecies, G. corvus bakilana ssp. nov., emphasizing that this taxon may be elevated to species status in the future pending new data. This biogeographic pattern, with apparently disjunct sister lineages in the South vs. North West of Madagascar, is rare among Malagasy anurans and calls for increased exploration of the remaining humid forest fragments in the North West and West of the island.

References

  1. Blommers-Schlösser, R.M.A. (1979) Biosystematics of the Malagasy frogs. I. Mantellinae (Ranidae). Beaufortia, 352, 1–77. [https://www.repository.naturalis.nl/document/548811]
  2. 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
  3. Brown, J.L., Cameron, A., Yoder, A.D. & Vences, M. (2014) A necessarily complex model to explain the biogeography of the amphibians and reptiles of Madagascar. Nature Communications, 5, e5046. https://doi.org/10.1038/ncomms6046
  4. 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
  5. Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Multi and single locus DNA fingerprinting. In: Molecular analysis of populations: A practical approach. IRL Press, Oxford, pp. 225–269.
  6. Cocca, W., Andreone, F., Belluardo, F., Rosa, G.M., Randrianirina, J.E., Glaw, F. & Crottini, A. (2020) Resolving a taxonomic and nomenclatural puzzle in mantellid frogs: synonymization of Gephyromantis azzurrae with G. corvus, and description of Gephyromantis kintana sp. nov. from the Isalo Massif, western Madagascar. Zookeys, 951, 133–157. https://doi.org/10.3897/zookeys.951.51129
  7. Cocca, W., Rosa, G.M., Andreone, F., Aprea, G., Eusebio Bergò, P., Mattioli, F., Mercurio, V., Randrianirina, J.E., Rosado, D., Vences, M. & Crottini, A. (2018) The herpetofauna (Amphibia, Crocodylia, Squamata, Testudines) of the Isalo Massif, Southwest Madagascar: combining morphological, molecular and museum data. Salamandra, 54, 178–200.
  8. Crottini, A., Glaw, F., Casiraghi, M., Jenkins, R.K.B., Mercurio, V., Randrianantoandro, C., Randrianirina, J.E. & Andreone, F. (2011) A new Gephyromantis (Phylacomantis) frog species from the pinnacle karst of Bemaraha, western Madagascar. Zookeys, 81, 51–71. https://doi.org/10.3897/zookeys.81.1111
  9. de Queiroz, K. (2020) An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetological Review, 51, 459–461.
  10. Dufresnes, C., Poyarkov, N. & Jablonski, D. (2023) Acknowledging more biodiversity without more species. Proceedings of the National Academy of Sciences of the United States of America, 120, e2302424120. https://doi.org/10.1073/pnas.2302424120
  11. Fedosov, A., Achaz, G., Gontchar, A. & Puillandre, N. (2022) Mold, a novel software to compile accurate and reliable DNA diagnoses for taxonomic descriptions. Molecular Ecology Resources, 22, 2038–2053. https://doi.org/10.1111/1755-0998.13590
  12. Frost, D.R. (2024) Amphibian Species of the World: an Online Reference. Version 6.2. American Museum of Natural History, New York, New York, Electronic Database. Available from: https://amphibiansoftheworld.amnh.org/ (accessed 12 March 2024)
  13. Glaw, F. & Vences, M. (2006) Phylogeny and genus-level classification of mantellid frogs (Amphibia, Anura). Organisms, Diversity & Evolution, 6, Electronic Supplement 11 (Part 1 & Part 2), 236–253, 1–3 & 1–4. https://doi.org/10.1016/j.ode.2005.12.001
  14. Glaw, F. & Vences, M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar. 3rd Edition. Vences & Glaw Verlag, Cologne, 496 pp.
  15. 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/10.1080/00222930050020140
  16. IUCN SSC Amphibian Specialist Group. (2016) Gephyromantis corvus. The IUCN Red List of Threatened Species, 2016, e.T57473A84170678. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T57473A84170678.en
  17. Kaffenberger, N., Wollenberg, K.C., Köhler, J., Glaw, F., Vieites, D.R. & Vences, M. (2012) Molecular phylogeny and biogeography of Malagasy frogs of the genus Gephyromantis. Molecular Phylogenetics and Evolution, 62, 555–560. https://doi.org/10.1016/j.ympev.2011.09.023
  18. 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
  19. 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
  20. 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
  21. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
  22. 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
  23. 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.
  24. Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21, 609–620. https://doi.org/10.1111/1755-0998.13281
  25. Rakotondravony, H. & Goodman, S.M. (2011) Rapid herpetofaunal surveys within five isolated forests on sedimentary rock in western Madagascar. Herpetological Conservation and Biology, 6, 297–311.
  26. Rambaut, A. (2018) FigTree. Version 1.4.4. Available from: https://github.com/rambaut/figtree/releases (accessed 25 March 2024)
  27. Randrianiaina, R.-D., Glaw, F., Thomas, M., Glos, J., Raminosoa, N. & Vences, M. (2007) Descriptions of the tadpoles of two species of Gephyromantis, with a discussion of the phylogenetic origin of direct development in mantellid frogs. Zootaxa, 1401, 53–61. https://doi.org/10.11646/zootaxa.1401.3
  28. Raselimanana, A.P. (2013) Faune herpétologique de la forêt de Beanka, Région Melaky: richesse biologique, intérêt biogéographique et importance dans la conservation de la biodiversité malgache. Malagasy Nature, 7, 209–224.
  29. Reeve, E., Ndriantsoa, S.H., Strauß, A., Randrianiaina, R.-D., Rasolonjatovo Hiobiarilanto, T., Glaw, F., Glos, J. & Vences, M. (2011) Acoustic underwater signals with a probable function during competitive feeding in a tadpole. Naturwissenschaften, 98, 135–143. https://doi.org/10.1007/s00114-010-0752-1
  30. Rodríguez, A., Börner, M., Pabijan, M., Gehara, M., Haddad, C.F.B. & Vences, M. (2015) Genetic divergence in tropical anurans: deeper phylogeographic structure in forest specialists and in topographically complex regions. Evolutionary Ecology, 29, 765–785. https://doi.org/10.1007/s10682-015-9774-7
  31. 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
  32. 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
  33. Scherz, M.D., Vences, M., Borrell, J., Ball, L., Nomenjanahary, D.H., Parker, D., Rakotondratsima, M., Razafimandimby, E., Starnes, T., Rabearivony, J. & Glaw, F. (2017) A new frog species of the subgenus Asperomantis (Anura: Mantellidae: Gephyromantis) from the Bealanana District of northern Madagascar. Zoosystematics and Evolution, 93, 451–466. https://doi.org/10.3897/zse.93.14906
  34. Scherz, M.D., Crottini, A., Hutter, C.R., Hildenbrand, A., Andreone, F., Fulgence, T.R., Köhler, G., Ndriantsoa, S.H., Ohler, A., Preick, M., Rakotoarison, A., Rancilhac, L., Raselimanana, A.P., Riemann, J.C., Rödel, M.O., Rosa, G.M., Streicher, J.W., Vieites, D.R., Köhler, J., Hofreiter, M., Glaw, F. & Vences, M. (2022) An inordinate fondness for inconspicuous brown frogs: integration of phylogenomics, archival DNA analysis, morphology, and bioacoustics yields 24 new taxa in the subgenus Brygoomantis (genus Mantidactylus) from Madagascar. Megataxa, 7 (2), 113–311. https://doi.org/10.11646/megataxa.7.2.1
  35. Scherz, M.D., Schmidt, L., Crottini, A., Miralles, A., Rakotoarison, A., Raselimanana, A.P., Köhler, J., Glaw, F. & Vences, M. (2021) Into the Chamber of Horrors: A proposal for the resolution of nomenclatural chaos in the Scaphiophryne calcarata complex (Anura: Microhylidae), with a new species-level phylogenetic hypothesis for Scaphiophryninae. Zootaxa, 4938 (4), 392–420. https://doi.org/10.11646/zootaxa.4938.4.2
  36. 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
  37. 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
  38. Vences, M., Andreone, F., Glos, J. & Glaw, F. (2010) Molecular and bioacoustic differentiation of Boophis occidentalis with description of a new treefrog from north-western Madagascar. Zootaxa, 2544 (1), 54–68. https://doi.org/10.11646/zootaxa.2544.1.2
  39. Vences, M. & Glaw, F. (2002) Molecular phylogeography of Boophis tephraeomystax: a test case for east-west vicariance in Malagasy anurans (Amphibia, Anura, Mantellidae). Spixiana, 25, 79–84.
  40. Vences, M., Köhler, J., Vieites, D.R. & Glaw, F. (2011) Molecular and bioacoustic differentiation of deep conspecific lineages of the Malagasy treefrogs Boophis tampoka and B. luteus. Herpetology Notes, 4, 239–246.
  41. Vences, M., Köhler, J., Pabijan, M., Bletz, M.C., Gehring, P.-S., Hawlitschek, O., Rakotoarison, A., Ratsoavina, F.M., Andreone, F., Crottini, A. & Glaw, F. (2017) Taxonomy and geographic distribution of Malagasy frogs of the Gephyromantis asper clade, with description of a new subgenus and revalidation of Gephyromantis ceratophrys. Salamandra, 53, 77–98.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
  42. Vences, M., Miralles, A. & Dufresnes, C. (2024) Next-generation species delimitation and taxonomy: Implications for biogeography. Journal of Biogeography. [published online] https://doi.org/10.1111/jbi.14807
  43. Vences, M., Multzsch, M., Köhler, J., Crottini, A., Andreone, F.., Rakotoarison, A., Scherz, M.D. & Glaw, F. (2023) Integrative revision of the Blommersia wittei complex, with description of a new species of frog from western and north-western Madagascar. Zootaxa, 5319 (2), 178–198. https://doi.org/10.11646/zootaxa.5319.2.2
  44. 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
  45. Vieites, D.R., Min, M.S. & Wake, D.B. (2007) Rapid diversification and dispersal during periods of global warming by plethodontid salamanders. Proceedings of the National Academy of Sciences of the United States of America, 104, 19903–19907. https://doi.org/10.1073/pnas.0705056104
  46. 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 United States of America, 106, 8267–8272. https://doi.org/10.1073/pnas.0810821106