Abstract
Madagascar velvet geckos, genus Blaesodactylus, are classified in six species distributed over low-elevation sites across most of Madagascar. Based on DNA sequences of one mitochondrial and two nuclear-encoded gene fragments obtained from numerous newly collected tissue samples, we provide an updated review of their molecular variation. Our genetic screening confirms an extended distribution of B. ambonihazo, so far only known from its type locality Ankarafantsika, now reaching northwards to the Sahamalaza Peninsula. Compared to previously available molecular data, we also verify minor range extensions of B. boivini (southeastwards to Bezavona), B. antongilensis (northwards to the Marojejy Massif), and the B. sakalava complex. Samples assigned to B. sakalava according to current taxonomy fell into two mitochondrial sister lineages differing by about 8.5% pairwise distances in the 16S rRNA gene, lack of haplotype sharing in the nuclear-encoded CMOS gene, and various subtle but consistent differences in body proportions and scalation. We conclude that the lineage occurring in the South of Madagascar, encompassing known locations south of Morombe, corresponds to B. sakalava sensu stricto based on its type locality and morphological characters of its name-bearing type; and describe the lineage occurring in the West of Madagascar north of Morombe as a new species, B. ganzhorni sp. nov.
References
- Arevalo, E., Davis, S.K. & Sites, J.W.Jr. (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Systematic Biology, 43, 387–418. https://doi.org/10.1093/sysbio/43.3.387
- 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. https://doi.org/10.1073/pnas.94.15.7748
- 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
- Bauer, A.M., Glaw, F., Gehring, P.-S. & Vences, M. (2011) New species of Blaesodactylus (Squamata: Gekkonidae) from Ankarafantsika National Park in north-western Madagascar. Zootaxa, 2942 (1), 57–68. https://doi.org/10.11646/zootaxa.2942.1.2
- Bauer, A.M., Scherz, M.D., Crottini, A., Ratsoavina, F.M. & Glaw, F. (2022) Gekkonidae, Geckos, Katsatsaka, TsaTsake. In: Goodman, S.M. (Ed.), The New Natural History of Madagascar. Princeton University Press, Princeton, New Jersey, pp. 1474–1479. https://doi.org/10.2307/j.ctv2ks6tbb.211
- Bell, J. (2008) A simple way to treat PCR products prior to sequencing using ExoSAP-IT. Biotechniques, 44, 834. https://doi.org/10.2144/000112890
- Böhme, W. & Meier, H. (1980) Revision der madagassischen Homopholis (Blaesodactylus)-Arten (Sauria: Gekkonidae). Senckenbergiana Biologica, 60, 303–315. [1979]
- Boulenger, G.A. (1896) Descriptions of new lizards from Madagascar. Annals and Magazine of Natural History, Series 6, 17, 444–446. https://doi.org/10.1080/00222939608680395
- 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
- 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.
- Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
- 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.
- de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886. https://doi.org/10.1080/10635150701701083
- Duméril, A.H.A. (1856) Description des reptiles nouveaux ou imparfaitement connus de la collection du Muséum d’Histoire Naturelle et remarques sur la classification et les caractères des reptiles. Archives du Muséum d'Histoire Naturelle de Paris, 8, 438–588.
- Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2020) 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
- Gehring, P.S., Ratsoavina, F.M. & Vences, M. (2010) Filling the gaps – amphibian and reptile records from lowland rainforests in eastern Madagascar. Salamandra, 46, 214–234.
- Gehring, P.S., Siarabi, S., Scherz, M.D., Ratsoavina, F.M., Rakotoarison, A., Glaw, F. & Vences, M. (2018) Genetic differentiation and species status of the large-bodied leaf-tailed geckos Uroplatus fimbriatus and U. giganteus. Salamandra, 54, 132–146.
- Glaw, F., Gehring, P.-S., Köhler, J., Franzen, M. & Vences, M. (2010) A new dwarf species of day gecko, genus Phelsuma, from the Ankarana pinnacle karst in northern Madagascar. Salamandra, 46, 83–92.
- Glaw, F., Köhler, J. & Vences, M. (2018) Three new species of nocturnal geckos of the Paroedura oviceps clade from xeric environments of Madagascar (Squamata: Gekkonidae). Zootaxa, 4433 (2), 305–324. https://doi.org/10.11646/zootaxa.4433.2.4
- Glaw, F., Rösler, H., Ineich, I., Gehring, P.-S., Köhler, J. & Vences, M. (2014) A new species of nocturnal gecko (Paroedura) from karstic limestone in northern Madagascar. Zoosystematics and Evolution, 90, 249–259. https://doi.org/10.3897/zse.90.8705
- Grandidier, A. (1867) Liste des reptiles nouveaux découverts, en 1866, sur la côte sud-ouest de Madagascar. Revue et Magazine de Zoologie, Paris, Série 2, 19, 232–234
- Greenbaum, E., Jackman, T. & Bauer, A.M. (2007) Homopholis and Blaesodactylus (Squamata: Gekkonidae) revisited: new insights from a molecular phylogeny. African Journal of Herpetology, 56, 101–114. https://doi.org/10.1080/21564574.2007.9635557
- Han, D., Zhou, K. & Bauer, A.M. (2004) Phylogenetic relationships among gekkotan lizards inferred from c-mos nuclear DNA sequences and a new classification of the Gekkota. Biological Journal of the Linnean Society, 83, 353–368. https://doi.org/10.1111/j.1095-8312.2004.00393.x
- Ikeuchi, I. & Mori, A. (2014) Natural history of a Madagascan gecko Blaesodactylus ambonihazo in a dry deciduous forest. Current Herpetology, 33, 161–170. https://doi.org/10.5358/hsj.33.161
- Ineich, I. & Bourgoin, T. (2016) Sex and food in a cave during daytime, a possible way to escape predators for the nocturnal Madagascar gekkonid Paroedura tanjaka Nussbaum & Raxworthy, 2000. Herpetology Notes, 9, 187–190.
- Ineich, I., Glaw, F. & Vences, M. (2016) A new species of Blaesodactylus (Squamata: Gekkonidae) from Tsingy limestone outcrops in Namoroka National Park, north-western Madagascar. Zootaxa, 4109 (5), 523–541. https://doi.org/10.11646/zootaxa.4109.5.2
- Jackman, T.R., Bauer, A.M., Greenbaum, E., Glaw, F. & Vences, M. (2008) Molecular phylogenetic relationships among species of the Mal-agasy-Comoran gecko genus Paroedura (Squamata: Gekkonidae). Molecular Phylogenetics and Evolution, 46, 74–81. https://doi.org/10.1016/j.ympev.2007.10.018
- Jenkins, R.K.B., Tognelli, M.F., Bowles, P., Cox, N., Brown, J.L., Chan, L., Andreone, F., Andriamazava, A., Andriantsimanarilafy, R.R., Anjeriniaina, M., Bora, P., Brady, L.D., Hantalalaina, E.F., Glaw, F., Griffiths, R.A., Hilton-Taylor, C., Hoffmann, M., Katariya, V., Rabibisoa, N.H., Rafanomezantsoa, J., Rakotomalala, D., Rakotondravony, H., Rakotondrazafy, N.A., Ralambonirainy, J., Ramanamanjato, J.B., Randriamahazo, H., Randrianantoandro, J.C., Randrianasolo, H.H., Randrianirina, J.E., Randrianizahana, H., Raselimanana, A.P., Rasolohery, A., Ratsoavina, F.M., Raxworthy, C.J., Robsomanitrandrasana, E., Rollande, F., Van Dijk, P.P., Yoder, A.D. & Vences, M. (2014) Extinction risks and the conservation of Madagascar’s reptiles. PLoS One, 9 (8), e100173. https://doi.org/10.1371/journal.pone.0100173
- Jono, T., Bauer, A.M., Brennan, I. & Mori, A. (2015) New species of Blaesodactylus (Squamata: Gekkonidae) from Tsingy karstic outcrops in Ankarana National Park, northern Madagascar. Zootaxa, 3980 (3), 406–416. https://doi.org/10.11646/zootaxa.3980.3.4
- 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
- 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 USA, 86, 6196–6200. https://doi.org/10.1073/pnas.86.16.6196
- Köhler, J., Vences, M., Scherz, M.D. & Glaw, F. (2019) A new species of nocturnal gecko, genus Paroedura, from the karstic Tsingy de Bemaraha formation in western Madagascar. Salamandra, 55 (2), 73–81.
- Kremen, C., Cameron, A., Moilanen, A., Phillips, S., 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., Wright, P.C. & 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, 1870–1874. https://doi.org/10.1093/molbev/msw054
- Lemme, I., Erbacher, M., Kaffenberger, N., Vences, M. & Köhler, J. (2013) Molecules and morphology suggest cryptic species diversity and an overall complex taxonomy of fish scale geckos, genus Geckolepis. Organisms Diversity and Evolution, 13, 87–95. https://doi.org/10.1007/s13127-012-0098-y
- Moat, J. & Smith, P. (2007) Atlas of the Vegetation of Madagascar. Royal Botanic Gardens, Kew Richmond, 124 pp.
- Miralles, A., Puillandre, N. Vences, M. (2024) Chapter 4. DNA barcoding in species delimitation: from genetic distances to integrative taxonomy. In: de Salle, R. (Ed.), DNA barcodes: methods and protocols. Springer protocol series. Humana, New York, New York, pp. 77–104. https://doi.org/10.1007/978-1-0716-3581-0_4
- Mohan, A.V., Gehring, P.S., Scherz, M.D., Glaw, F., Ratsoavina, F.M. & Vences, M. (2019) Comparative phylogeography and patterns of deep genetic differentiation of two gecko species, Paroedura gracilis and Phelsuma guttata, across north-eastern Madagascar. Salamandra, 55, 211–220.
- Nachman, M.W., Beckman, E.J., Bowie, R.C., Cicero, C., Conroy, C.J., Dudley, R., Hayes, T.B., Koo, M.S., Lacey, E.A., Martin, C.H., McGuire, J.A., Patton, J.L., Spencer, C.L., Tarvin, R.D., Wake, M.H., Wang, I.J., Achmadi, A., Álvarez-Castañeda, S.T., Andersen, M.J., Arroyave, J., Austin, C.C., Barker, F.K., Barrow, L.N., Barrowclough, G.F., Bates, J., Bauer, A.M., Bell, K.C., Bell, R.C., Bronson, A.W., Brown, R.M., Burbrink, F.T., Burns, K.J., Cadena, C.D., Cannatella, D.C., Castoe, T.A., Chakrabarty, P., Colella, J.P., Cook, J.A., Cracraft, J.L., Davis, D.R., Davis Rabosky, A.R., D'Elía, G., Dumbacher, J.P., Dunnum, J.L., Edwards, S.V., Esselstyn, J.A., Faivovich, J., Fjeldså, J., Flores-Villela, O.A., Ford, K, Fuchs, J., Fujita, M.K., Good, J.M., Greenbaum, E., Greene, H.W., Hackett, S., Hamidy, A., Hanken, J., Haryoko, T., Hawkins, M.T., Heaney, L.R., Hillis, D.M., Hollingsworth, B.D., Hornsby, A.D., Hosner, P.A., Irham, M., Jansa, S., Jiménez, R.A., Joseph, L., Kirchman, J.J., LaDuc, T.J., Leaché, A.D., Lessa, E.P., López-Fernández, H., Mason, N.A., McCormack, J.E., McMahan, C.D., Moyle, R.G., Ojeda, R.A., Olson, L.E., Kin Onn, C., Parenti, L.R., Parra-Olea, G., Patterson, B.D., Pauly, G.B., Pavan, S.E., Peterson, A.T., Poe, S., Rabosky, D.L., Raxworthy, C.J., Reddy, S., Rico-Guevara, A., Riyanto, A., Rocha, L.A., Ron, S.R., Rovito, S.M., Rowe, K.C., Rowley, J., Ruane, S., Salazar-Valenzuela, D., Shultz, A.J., Sidlauskas, B., Sikes, D.S., Simmons, N.B., Stiassny, M.L.J., Streicher, J.W., Stuart, B.L., Summers, A.P., Tavera, J., Teta, P., Thompson, C.W., Timm, R.M., Torres-Carvajal, O., Voelker, G., Voss, R.S., Winker, K., Witt, C., Wommack, E.A. & Zink, R.M. (2023) Specimen collection is essential for modern science. PLoS Biology, 21, e3002318. https://doi.org/10.1371/journal.pbio.3002318.
- Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, e16. https://doi.org/10.1186/1742-9994-7-16
- 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.
- Penny, S.G., Crottini, A., Andreone, F., Bellati, A., Rakotozafy, L.M.S, Holderied, M.W., Schwitzer, C. & Rosa, G.M. (2017) Combining old and new evidence to increase the known biodiversity value of the Sahamalaza Peninsula, Northwest Madagascar. Contributions to Zoology, 86 (4) 273–296. https://doi.org/10.1163/18759866-08604002
- Rakotoarimalala, F. & Raselimanana, A.P. (2023) Aperçu global de la tendance de la structure de la communauté herpétofaunique le long du gradient altitudinal du versant Est du Parc National de Marojejy au cours de ces 25 dernières années. In: Goodman, S.M. & Raherilalao, M.J. (Eds.), A floral and faunal inventory of the Parc National de Marojejy: Altitudinal gradient and temporal variation. Malagasy Nature, 17, pp. 165–186.
- Raselimanana, A.P. (2008) Herpétofaune des forêts sèches malgaches. Malagasy Nature, 1, 46–75.
- Ratsoavina, F.M., Scherz, M.D., Tolley, K.A., Raselimanana, A.P., Glaw, F. & Vences, M. (2019) A new species of Uroplatus (Gekkonidae) from Ankarana National Park, Madagascar, of remarkably high genetic divergence. Zootaxa, 4683 (1), 84–96. https://doi.org/10.11646/zootaxa.4683.1.4
- Rocha, S., Vences, M., Glaw, F., Posada, D. & Harris, D.J. (2009) Multigene phylogeny of Malagasy day geckos of the genus Phelsuma. Molecular Phylogenetics and Evolution, 52, 530–537. https://doi.org/10.1016/j.ympev.2009.03.032
- Russell, A.P. (1978) The status of the lizard genera Blaesodactylus Boettger and Homopholis Boulenger (Reptilia: Gekkonidae). Copeia, 1978, 25–29. https://doi.org/10.2307/1443817
- Scherz, M.D., Daza, J.D., Köhler, J., Vences, M. & Glaw, F. (2017) Off the scale: a new species of fish-scale gecko (Squamata: Gekkonidae: Geckolepis) with exceptionally large scales. PeerJ, 5, e2955. https://doi.org/10.7717/peerj.2955
- 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
- 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
- Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–635. https://doi.org/10.1093/genetics/132.2.619
- Uetz, P., Freed, P., Aguilar, R., Reyes, F., Kudera, J. & Hošek, J. (Eds.) (2024) The Reptile Database. Available from: http://www.reptile-database.org (accessed May 15 August 2024)
- 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., Miralles, A. & Dufresnes, C. (2024b) Next-generation species delimitation and taxonomy: implications for biogeography. Journal of Biogeography, 51 (9), 1709–1722. https://doi.org/10.1111/jbi.14807
- Vences, M., Multzsch, M., Gippner, S., Miralles, A., Crottini, A., Gehring, P.-S., Rakotoarison, A., Ratsoavina, F.M., Glaw, F. & Scherz, M.D. (2022b) Integrative revision of the Lygodactylus madagascariensis group reveals an unexpected diversity of little brown geckos in Madagascar’s rainforest. Zootaxa, 5179 (1), 1–61. https://doi.org/10.11646/zootaxa.5179.1.1
- Vences, M., Patmanidis, S., Kharchev, V. & Renner, S.S. (2022a) 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
- Vences, M., Patmanidis, S., Schmidt, J.-C., Matschiner, M., Miralles, A. & Renner, S.S. (2024a) Hapsolutely: a user-friendly tool integrating haplotype phasing, network construction and haploweb calculation. Bioinformatics Advances, vbae083. https://doi.org/10.1093/bioadv/vbae083