Abstract
The genus Scaphiophryne (Anura: Microhylidae) contains at least nine species that, together with their probable sister genus Paradoxophyla, form the Madagascar-endemic subfamily Scaphiophryninae. Scaphiophryne are robust burrowing frogs with explosive breeding behavior and are characterized by a unique larval morphology, being intermediate between that of filter-feeding and generalized tadpole types. Based on tadpole morphology, the nominal subgenus Scaphiophryne can be distinguished from the subgenus Pseudohemisus, a clade occurring in arid biomes with a largely unsolved taxonomy and nomenclature. Here we combine a comprehensive molecular phylogeny of all scaphiophrynines based on five mitochondrial and two nuclear genes with a re-examination of the name-bearing type specimens of the seven species-level nomina assignable to the subgenus Pseudohemisus. Our molecular phylogeny supports monophyly of the two subgenera and assigns the enigmatic S. matsoko to the subgenus Scaphiophryne. In this subgenus, our analysis confirms all currently accepted species as independent evolutionary lineages based on concordant differentiation in mitochondrial and nuclear genes, and provides evidence for a combination of low mitochondrial divergence, distinct nuclear divergence, and high nuclear heterozygosity. Yet, contrary to previous hypotheses, we do not find evidence of ongoing hybridization. In the subgenus Pseudohemisus we find support for three clearly delimited species-level lineages, one of which contains two deep conspecific lineages that warrant further study. To stabilize the taxonomy in this subgenus, and considering the very poor state of preservation of several type series and the heterogeneity of some of them, we here designate lectotypes for the nomina: Hemisus obscurus Grandidier, 1872; Calophrynus calcaratus Mocquard, 1895; Pseudohemisus verrucosus Angel, 1930; Pseudohemisus longimanus Angel, 1930; and Pseudohemisus longimanus var. melanopleura Angel, 1934. Taxonomically, we accept Scaphiophryne brevis (Boulenger, 1896) as a well-defined species; restrict S. calcarata (Mocquard, 1995) to the southern lineage of the S. calcarata complex; resurrect Hemisus obscurus Grandidier, 1872 (previously considered to be a dubious name or nomen inquirendum) as Scaphiophryne obscura to refer to the western and north-western lineage of the S. calcarata complex; consider Pseudohemisus verrucosus Angel, 1930 as junior synonym of Scaphiophryne brevis; and consider Pseudohemisus longimanus Angel, 1930 and Pseudohemisus longimanus var. melanopleura Angel, 1934 as junior synonyms of Scaphiophryne obscura. Finally, to accelerate taxonomic progress, we (i) outline a set of criteria by which such old and ambiguous nomina can be applied to known lineages, (ii) suggest that the International Code of Zoological Nomenclature should slightly broaden the conditions under which neotypes are to be designated, and (iii) propose to redouble discussions on the introduction of the concept of the epitype to zoology.
References
AmphibiaWeb (2020) AmphibiaWeb. University of California, Berkeley, California. Available from: https://amphibiaweb.org (accessed 7 June 2020)
Andreone, F., Bergò, P.E., Mercurio, V. & Rosa, G.M. (2013) Spatial ecology of Scaphiophryne gottlebei in the canyons of the Isalo Massif, Madagascar. Herpetologica, 69, 11–21.
https://doi.org/10.1655/HERPETOLOGICA-D-12-00005
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
Angel, F. (1930) Description de deux espèces nouvelles de batraciens de Madagascar, appartenant au genre Pseudohemisus. Bulletin du Museum National d’Histoire Naturelle, Paris, Serie 2, 2, 70–74.
Angel, F. (1934) Description d’un Vipéridé nouveau du Congo Belge et de deux batraciens de Madagascar. Bulletin de la Société Zoologique de France, 59, 169–172.
Ariyawansa, H.A., Hawksworth, D.L., Hyde, K.D., Jones, E.B.G., Maharachchikumbura, S.S.N., Manamgoda, D.S., Thambugala, K.M., Udayanga, D., Camporesi, E., Daranagama, A., Jayawardena, R., Liu, J.-K., McKenzie, E.H.C., Phookamsak, R., Senanayake, I.C., Shivas, R.G., Tian, Q. & Xu, J.-C. (2014) Epitypification and neotypification: guidelines with appropriate and inappropriate examples. Fungal Diversity, 69, 57–91.
https://doi.org/10.1007/s13225-014-0315-4
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
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.94.15.7748
Blommers-Schlösser, R.M.A. (1975) Observations on the larval development of some Malagasy frogs, with notes on their ecology and biology (Anura: Dyscophinae, Scaphiophryninae and Cophylinae). Beaufortia, 24 (309), 7–26.
Blommers-Schlösser, R.M.A. & Blanc, C.P. (1991) Amphibiens (première partie). Faune de Madagascar, 75 (1), 1–379.
Boulenger, G.A. (1896) Descriptions of new batrachians in the British Museum. Annals and Magazine of Natural History, Series 6, 17, 401–406.
https://doi.org/10.1080/00222939608680389
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.
Cocca, W., Rosa, G.M., Andreone, F., Aprea, G., Bergò, P.E., 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.
Crottini, A., Chiari, Y., Mercurio, V., Meyer, A., Vences, M. & Andreone, F. (2008) Into the canyons: the phylogeography of the Malagasy frogs Mantella expectata and Scaphiophryne gottlebei in the arid Isalo Massif, and its significance for conservation (Amphibia: Mantellidae and Microhylidae). Organisms Diversity and Evolution, 8, 368–377.
https://doi.org/10.1016/j.ode.2008.08.001
D’Cruze, N., Olsonn, A., Henson, D., Kumar, S. & Emmett, D. (2009) Amphibians and reptiles of the Onilahy River valley. Herpetological Conservation and Biology, 4, 62–79.
Evans, B.J., Gansauge, M.-T., Stanley, E.L., Furman, B.L.S., Cauret, C.M.S., Ofori-Boateng, C., Gvoždík, V., Streicher, J.W., Greenbaum, E., Tinsley, R.C., Meyer, M. & Blackburn, D.C. (2019) Xenopus fraseri: Mr. Fraser, where did your frog come from? PLoS One, 14, e0220892.
https://doi.org/10.1371/journal.pone.0220892
Frost, D.R. (2020) Amphibian Species of the World: an Online Reference. Version 6.1. Electronic Database accessible at American Museum of Natural History, New York. Available from: https://amphibiansoftheworld.amnh.org/index.php (accessed 7 June 2020)
https://doi.org/10.5531/db.vz.0001
Glaw, F. & Vences, M. (2007) A Field Guide to the Amphibians and Reptiles of Madagascar. Third Edition. Köln, Vences & Glaw, 496 pp.
Glos, J., Glaw, F. & Vences, M. (2005) A new species of Scaphiophryne from western Madagascar. Copeia, 2005, 252–261.
https://doi.org/10.1643/CH-04-238R2
Grandidier, A. (1872) Description de quelques reptiles nouveaux découverts à Madagascar en 1870. Annales des Sciences Naturelles. Zoologie et Paléontologie, Paris, Série 5, 15, 6–11.
Grosjean, S., Glos, J., Teschke, M., Glaw, F. & Vences, M. (2007) Comparative larval morphology of Madagascan toadlets of the genus Scaphiophryne: phylogenetic and taxonomic inferences. Zoological Journal of the Linnean Society, 151, 555–576.
https://doi.org/10.1111/j.1096-3642.2007.00329.x
Grosjean, S. & Vences, M. (2009) The tadpole of the toadlet Scaphiophryne marmorata from Madagascar. Zootaxa, 1986 (1), 67–68.
https://doi.org/10.11646/zootaxa.1986.1.3
Guibé, J. (1952) Recherches sur les batraciens de Madagascar. Mémoires de l’Institut Scientifique de Madagascar. Série A, Biologie Animale,7, 109–116.
Guibé, J. (1978) Les batraciens de Madagascar. Bonner zoologische Monographien, 11, 1–140.
Hawksworth, D.L. (2012) Addressing the conundrum of unavailable name-bearing types. IMA Fungus, 3, 155–158.
https://doi.org/10.5598/imafungus.2012.03.02.07
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.4251.1.1
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
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.
https://doi.org/10.1093/molbev/msw260
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
Mercurio, V. & Andreone, F. (2006) The tadpoles of Scaphiophryne gottlebei (Microhylidae, Scaphiophryninae) and Mantella expectata (Mantellidae, Mantellinae) from Isalo Massif, central-southern Madagascar. Alytes, 23, 81–95.
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
Miralles, A., Bruy, T., Wolcott, K., Scherz, M.D., Begerow, D., Beszteri, B., Bonkowski, M., Felden, J., Gemeinholzer, B., Glaw, F., Glöckner, F.O., Hawlitschek, O., Kostadinov, I., Nattkemper, T.W., Printzen, C., Renz, J., Rybalka, N., Stadler, M., Weibulat, T., Wilke, T., Renner, S.S. & Vences, M. (2020) Repositories for taxonomic data: where we are and what is missing. Systematic Biology, 69 (6), 1231–1253.
https://doi.org/10.1093/sysbio/syaa026
Mo, Y., Zhang, W., Zhou, S., Chen, T., Tang, H., Meng, Y. & Chen, W. (2013) A new species of Kaloula (Amphibia: Anura: Microhylidae) from southern Guangxi, China. Zootaxa, 3710 (2), 165–178.
https://doi.org/10.11646/zootaxa.3710.2.3
Moat, J. & Smith, P. (Eds.) (2007) Atlas of the vegetation of Madagascar. Kew Publishing, Kew, 124 pp.
Mocquard, F. (1895) Sur les reptiles recueillis Madascar de 1867 a 1885 par M. Grandidier. Bulletin de la Société Philomathique de Paris, Series 8, 7, 93–111.
Mosyakin, S.L. & McNeill, J. (2018) On the nomenclature of Chenopodium pallidum and Atriplex schugnanica (Chenopodiaceae/Amaranthaceae sensu APG) and the perils of epitypification. Phytotaxa, 376 (3), 133–137.
https://doi.org/10.11646/phytotaxa.376.3.2
Peloso, P.L.V., Frost, D.R., Richards, S.J., Rodrigues, M.T., Donnellan, S., Matsui, M., Raxworthy, C.J., Biju, S.D., Lemmon, E.M., Lemmon, A.R. & Wheeler, W.C. (2016) The impact of anchored phylogenomics and taxon sampling on phylogenetic inference in narrow-mouthed frogs (Anura, Microhylidae). Cladistics, 32, 113–140.
https://doi.org/10.1111/cla.12118
Prötzel, D., Scherz, M.D., Ratsoavina, F.M., Vences, M. & Glaw, F. (2020) Untangling the trees: Revision of the Calumma nasutum complex (Squamata: Chamaeleonidae). Vertebrate Zoology, 70, 23–59.
https://doi.org/10.26049/VZ70-1-2020-3
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., Scherz, M.D., Glaw, F., Köhler, J., Andreone, F., Franzen, M., Glos, J., Hawlitschek, O., Jono, T., Mori, A., Ndriantsoa, S.H., Raminosoa Rasoamampionona, 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.
Rancilhac, L., Bruy, T., Scherz, M.D., Almeida Pereira, E., Preick, M., Straube, N., Lyra, M.L., Ohler, A., Streicher, J.W., Andreone, F., Crottini, A., Hutter, C.R., Randrianantoandro, J.C., Rakotoarison, A., Glaw, F., Hofreiter, M. & Vences, M. (2020) Target-enriched DNA sequencing from historical type material enables a partial revision of the Madagascar giant stream frogs (genus Mantidactylus). Journal of Natural History, 54 (1–4), 1–12.
https://doi.org/10.1080/00222933.2020.1748243
Raselimanana, A.P. (2008) Herpétofaune des forets sèches malgaches. Malagasy Nature, 1, 46–75.
Raselimanana, A.P., Raxworthy, C.J., Andreone, F., Glaw, F. & Vences, M. (2014) An enigmatic new Scaphiophryne toadlet from the rainforests of north-eastern Madagascar (Amphibia: Microhylidae). Vertebrate Zoology, 64, 95–102.
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
Rosa, G.M., Mercurio, V., Crottini, A. & Andreone, F. (2011) Explosion into the canyon: breeding aggregation in Scaphiophryne gottlebei Busse & Böhme, 1992. North-Western Journal of Zoology, 7, 329–333.
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
Sánchez-Nivicela, J.C., Peloso, P.L.V., Urgiles, V.L., Yánez-Muñoz, M.H., Sagredo, Y., Páez, N. & Ron, S. (2020) Description and phylogenetic relationships of a new trans-Andean species of Elachistocleis Parker 1927 (Amphibia, Anura, Microhylidae). Zootaxa, 4779 (3), 323–340.
https://doi.org/10.11646/zootaxa.4779.3.2
Scherz, M.D., Hutter, C.R., Rakotoarison, A., Riemann, J.C., Rödel, M.-O., Ndriantsoa, S.H., Glos, J., Hyde Roberts, S., Crottini, A., Vences, M. & Glaw, F. (2019) Morphological and ecological convergence at the lower size limit for vertebrates highlighted by five new miniaturised microhylid frog species from three different Madagascan genera. PLoS ONE, 14, e0213314.
https://doi.org/10.1371/journal.pone.0213314
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
Scherz, M.D., Hawlitschek, O., Andreone, F., Rakotoarison, A., Vences, M. & Glaw, F. (2017a) 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.4273.3.1
Scherz, M.D., Vences, M., Rakotoarison, A., Andreone, F., Köhler, J., Glaw, F. & Crottini, A. (2017b) Lumping or splitting in the Cophylinae (Anura: Microhylidae) and the need for a parsimony of taxonomic changes: a response to Peloso et al. (2017). Salamandra, 53, 479–483.
Scherz, M.D., Rasolonjatovo, S.M., Köhler, J., Rancilhac, L., Rakotoarison, A., Raselimanana, A.P., Ohler, A., Preick, M., Hofreiter, M., Glaw, F. & Vences, M. (2020) Overcoming extrinsic hindrances to taxonomic progress: archival DNA from historical type material enables the description of a new microendemic frog species from north Madagascar. Scientific Reports, 10, 19109.
https://doi.org/10.1038/s41598-020-75431-9
Schrödl, M. & Haszprunar, G. (2014) Do we need epitypes in zoology? Spixiana, 39, 199–201.
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
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
Streicher, J.W., Loader, S.P., Varela-Jaramillo, A., Montoya, P. & de Sá, R.O. (2020) Analysis of ultraconserved elements supports African origins of narrow-mouthed frogs. Molecular Phylogenetics and Evolution, 146, 106771.
https://doi.org/10.1016/j.ympev.2020.106771
Tu, N., Yang, M., Liang, D. & Zhang, P. (2018) A large-scale phylogeny of Microhylidae inferred from a combined dataset of 121 genes and 427 taxa. Molecular Phylogenetics and Evolution, 126, 85–91.
https://doi.org/10.1016/j.ympev.2018.03.036
Van der Meijden, A., Vences, M., Hoegg, S., Boistel, R. Channing, A. & Meyer, A. (2007) Nuclear gene phylogeny of narrow-mouthed toads (Family: Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Molecular Phylogenetics and Evolution, 44, 1017–1030.
https://doi.org/10.1016/j.ympev.2007.02.008
Vences, M., Aprea, G., Capriglione, T., Andreone, F. & Odierna, G. (2002a) Ancient tetraploidy and slow molecular evolution in Scaphiophryne: ecological correlates of speciation mode in Malagasy relict amphibians. Chromosome Research, 10, 127–136.
https://doi.org/10.1023/A:1014949001810
Vences, M., Andreone, F., Glaw, F., Raminosoa, N., Randrianirina, J.E. & Vieites, D.R. (2002b) Amphibians and reptiles of the Ankaratra Massif: reproductive diversity, biogeography and conservation of a montane fauna in Madagascar. Italian Journal of Zoology, 69, 263–284.
https://doi.org/10.1080/11250000209356469
Vences, M., Glaw, F. & Marquez, R. (Eds.) (2006) The Calls of the Frogs of Madagascar. 3 Audio CD’s and booklet. Fonoteca Zoológica, Madrid, 44 pp.
Vences, M., Guayasamin, J.M., Miralles, A. & de la Riva, I. (2013) To name or not to name: Criteria to promote economy of change in Linnaean classification schemes. Zootaxa, 3636 (2), 201–244.
https://doi.org/10.11646/zootaxa.3636.2.1
Vences, M., Raxworthy, C.J., Nussbaum, R.A. & Glaw, F. (2003) A revision of the Scaphiophryne marmorata complex of marbled toads from Madagascar, including the description of a new species. Herpetological Journal, 13, 69–79.
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
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
Wassersug, R.J. (1984) The Pseudohemisus tadpole: a morphological link between microhylid (Orton type 2) and ranoid (Orton type 4) larvae. Herpetologica, 40, 138–149.
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.