Advertisement

Organisms Diversity & Evolution

, Volume 15, Issue 1, pp 175–198 | Cite as

Morphology and molecules reveal two new species of the poorly studied gecko genus Paragehyra (Squamata: Gekkonidae) from Madagascar

  • Angelica CrottiniEmail author
  • D. James Harris
  • Aurélien Miralles
  • Frank Glaw
  • Richard K. B. Jenkins
  • J. Christian Randrianantoandro
  • Aaron M. Bauer
  • Miguel Vences
Original Article

Abstract

We provide new morphological and genetic data on a poorly studied genus of geckos from Madagascar (Paragehyra) previously thought to be distributed only in the south-east and south-west of the island and discuss the biogeography and evolution of this genus. Two species (Paragehyra petiti and Paragehyra gabriellae) were formerly included in this genus, whose phylogenetic and biogeographical relationships remain unresolved. This morphological and molecular study enables the recognition of two new rock-dwelling species that are here formally described. Paragehyra felicitae sp. nov. has only been observed in the private Anja reserve and nearby areas (close to Ambalavao) on the southern central high plateau of Madagascar, whereas Paragehyra austini sp. nov. is known from only one locality on the western slopes of the Andohahela massif, around 60 km northwest of Tolagnaro. The four species differ from one another by a combination of several morphological characters, genetic divergence >5.2 % in a mitochondrial 16S ribosomal RNA (rRNA) gene fragment and nucleotide differences in analysed nuclear genes, as highlighted in the resulting phylogenetic reconstruction and haplotype network analysis. A further, hitherto unstudied Paragehyra population is known from the Tsingy de Bemaraha in central-western Madagascar. Preliminary information of its morphological differentiation are here provided and suggest that this undescribed species is closely related to P. petiti and P. felicitae sp. nov.

Keywords

Paragehyra felicitae sp. nov. Paragehyra austini sp. nov. Systematics Phylogenetics Taxonomy Rock-dwelling geckos 

Notes

Acknowledgments

We are grateful to the community managing the Anja reserve for the permit to collect a limited number of reptiles thereby allowing the discovery of a remarkable local endemism of reptiles at this site. For help in the field, we are indebted to our Malagasy assistant Emile Rajeriarison and to our colleagues Iker A. Irisarri, Solohery Rasamison, Fanomezana Ratsoavina and Alexandra Lima as well as to many local porters and guides who accompanied us in the field. The work was carried out in collaboration with the Département de Biologie Animale, Université d’Antananarivo (UADBA). We are grateful to the Malagasy authorities, in particular the Ministère de l’Environnement et des Forêts, for issuing research and export permits (Nos. 195/09/MEF/SG/DGEF/DSAP/SLRSE, 292 MINENVEF/SG/DGEF/DPB/SCBLF/RECH, 128/06/MINENV.EF/SG/DGEF/DPB/SCBLF/RECH and 314/10/MEF/SG/DGF/DCB.SAP/SCB, 052N_EA02/MG05, 055N-EA03/MG10 and 007N_EA01/MG11). Fieldwork was partially funded by the Portuguese “Fundação para a Ciência e Tecnologia” (FCT) (PTDC/BIA-BDE/65745/2006). The work of AC was supported by postdoctoral grants from the Portuguese “Fundacao para a Ciencia e a Tecnologia” (FCT) (SFRH/BPD/72908/2010 and SFRH/BPD/96982/2013) under the Programa Operacional Potencial Humano–Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência. DJH and AC are funded by the project “Genomics and Evolutionary Biology” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2–O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF). The work of AM was supported by a postdoctoral research fellowship of the Alexander von Humboldt Foundation. Fieldwork of FG and MV was supported by the Volkswagen Foundation, and MV was supported by the Deutsche Forschungsgemeinschaft (grant VE247/3-1). AMB was supported by the National Science Foundation (USA) (grants DEB 0844523 and DEB 1019443), and RKBJ and JCR were funded by the Darwin Initiative.

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

13127_2014_191_Fig7_ESM.jpg (4.4 mb)
Fig. S1

(a) Anja Reserve, type locality of P. felicitae sp. nov. and an overview of the surrounding exploited areas; (b−d). second locality of P. felicitae sp. nov characterized by big granitic boulders that face the reserve from the other side of national road N7. In the background of figure (b) is Anja Reserve. (a) photo by AC; (b−d) photos by AM. (JPEG 4469 kb)

References

  1. Ali, J. R., & Aitchison, J. C. (2008). Gondwana to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma). Earth-Science Reviews, 88, 145–166.CrossRefGoogle Scholar
  2. Angel, F. (1929). Description d’un gecko nouveau, de Madagascar. Bulletin de la Société Zoologique de France, 54, 489–491.Google Scholar
  3. Bora, P., Randrianantoandro, J. C., Randrianavelona, R., Hantalalaina, E. F., Andriantsimanarilafy, R. R., Rakotondravony, D., Ramilijaona, O. R., Vences, M., Jenkins, R. K. B., Glaw, F., & Köhler, J. (2010). Amphibians and reptiles of the Tsingy de Bemaraha Plateau, Western Madagascar: checklist, biogeography and conservation. Herpetological Conservation and Biology, 5, 111–125.Google Scholar
  4. Bruford, M. W., Hanotte, O., Brookfield, J. F. Y., & Burke, T. (1992). Single locus and multilocus DNA fingerprint. In A. R. Hoelzel (Ed.), Molecular genetic analysis of populations: a practical approach (pp. 225–270). Oxford: IRL Press.Google Scholar
  5. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.CrossRefPubMedGoogle Scholar
  6. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.CrossRefPubMedGoogle Scholar
  7. Crottini, A., Gehring, P.-S., Glaw, F., Harris, D. J., Lima, A., & Vences, M. (2011). Deciphering the cryptic species diversity of dull-colored day gekos Phelsuma (Squamata: Gekkonidae) from Madagascar, with description of a new species. Zootaxa, 2982, 340–348.Google Scholar
  8. Crottini, A., Madsen, O., Poux, C., Strauß, A., Vieites, D. R., & Vences, M. (2012a). Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proceedings of the National Academy of Sciences of the USA, 109(14), 5358–5363.CrossRefPubMedCentralPubMedGoogle Scholar
  9. Crottini, A., Miralles, A., Glaw, F., Harris, D. J., Lima, A., & Vences, M. (2012b). Description of a new pygmy chameleon (Chamaeleonidae: Brookesia) from central Madagascar. Zootaxa, 3490, 63–74.Google Scholar
  10. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772.CrossRefPubMedGoogle Scholar
  11. Gamble, T., Greenbaum, E., Russell, A. P., Jackman, T. R., & Bauer, A. M. (2012). Repeated origin and loss of toepads in geckos. PLoS ONE, 7(6), e39429.CrossRefPubMedCentralPubMedGoogle Scholar
  12. Gehring, P.-S., Tolley, K. A., Eckhardt, F. S., Townsend, T. M., Ziegler, T., Ratsoavina, F., Glaw, F., & Vences, M. (2012). Hiding deep in the trees: discovery of divergent mitochondrial lineages in Malagasy chameleons of the Calumma nasutum group. Ecology and Evolution, 2, 1468–1479.CrossRefPubMedCentralPubMedGoogle Scholar
  13. Glaw, F., & Schmidt, K. (2003). Beobachtungen an Paragehyra petiti, einem lange Zeit verschollenen Gecko aus Madagaskar (Sauria: Gekkonidae). Gekkota, 4, 34–39.Google Scholar
  14. Glaw, F. & Vences, M. (2007). A field guide to the amphibians and reptiles of Madagascar, third edition. Vences & Glaw Verlag, Köln (Cologne), 496 ppGoogle Scholar
  15. Glaw, F., Köhler, J., & Vences, M. (2009a). A new species of cryptically coloured day gecko (Phelsuma) from the Tsingy de Bemaraha National Park in western Madagascar. Zootaxa, 2195, 61–68.Google Scholar
  16. Glaw, F., Nagy, Z. T., Köhler, J., Franzen, M., & Vences, M. (2009b). Phylogenetic relationships of a new species of pseudoxyrhophiine snake (Reptilia: Lamprophiidae: Thamnosophis) suggest a biogeographical link between western and northern Madagascar. Organisms Diversity and Evolution, 9, 13–22.CrossRefGoogle Scholar
  17. Goodman, S. M., & Benstead, J. P. (2003). The natural history of Madagascar (p. 1709). Chicago: The University of Chicago Press.Google Scholar
  18. Hoegg, S., Vences, M., Brinkmann, H., & Meyer, A. (2004). Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Molecular Biology and Evolution, 21, 1188–1200.CrossRefPubMedGoogle Scholar
  19. IUCN (2001). IUCN red list categories and criteria. Version 3.1. IUCN Species Survival Commission, IUCN, Gland, Switzerland and Cambridge, United Kingdom, 30 pp.Google Scholar
  20. IUCN (2012). IUCN Red List of threatened species. Version 2012.1. www.iucnredlist.org Downloaded on 01 August 2012.
  21. Jobb, G. (2011). TREEFINDER version of March 2011. Munich, Germany. Distributed by the author at www.treefinder.de.
  22. Kluge, A. G., & Nussbaum, R. A. (1995). A review of African-Madagascan gekkonid lizard phylogeny and biogeography (Squamata). Miscellaneous Publications Museum of Zooogy, University of Michigan, 183, i−iv +1−20.Google Scholar
  23. Lanfear, R., Calcott, B., Ho, S., & Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.CrossRefPubMedGoogle Scholar
  24. Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.CrossRefPubMedGoogle Scholar
  25. Lima, A., Harris, D. J., Rocha, S., Miralles, A., Glaw, F., & Vences, M. (2013). Phylogenetic relationships of Trachylepis skink species from Madagascar and the Seychelles (Squamata: Scincidae). Molecular Phylogenetics and Evolution, 67, 615–620.CrossRefPubMedGoogle Scholar
  26. Miralles, A., & Vences, M. (2013). New metrics for comparison of taxonomies reveal striking discrepancies among species delimitation methods in Madascincus lizards. PLoS ONE, 8, e68242.CrossRefPubMedCentralPubMedGoogle Scholar
  27. Münchenberg, T., Wollenberg, K. C., Glaw, F., & Vences, M. (2008). Molecular phylogeny and geographic variation of Malagasy iguanas (Oplurus and Chalarodon). Amphibia-Reptilia, 29, 319–327.CrossRefGoogle Scholar
  28. Nagy, Z. T., Sonet, G., Glaw, F., & Vences, M. (2012). First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. PLoS ONE, 7, e34506.CrossRefPubMedCentralPubMedGoogle Scholar
  29. Nussbaum, R. A., & Raxworthy, C. J. (1994). The genus Paragehyra (Reptilia: Sauria: Gekkonidae) in southern Madagascar. Journal of Zoology, 232, 37–59.CrossRefGoogle Scholar
  30. Nussbaum, R. A., & Raxworthy, C. J. (2000). Systematic revision of the genus Paroedura Günther (Reptilia: Squamata: Gekkonidae), with description of five new species. Miscellaneous Publications, Museum of Zoology, University of Michigan, 189, 1–26.Google Scholar
  31. Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L., & Grabowski, G. (1991). The simple fool’s guide to PCR. Honolulu: Department of Zoology.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. Pyron, R. A., Burbrink, F. T., & Wiens, J. J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93.CrossRefPubMedCentralPubMedGoogle Scholar
  34. Rambaut, A. & Drummond, A. J. (2007). Tracer v1.5, <http://beast.bio.ed.ac.uk/Tracer>.
  35. Raselimanana, A. P. (2008). Herpétofaune des forets sèches malgaches. Malagasy Nature, 1, 46–75.Google Scholar
  36. 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(3), 539–542.CrossRefPubMedCentralPubMedGoogle Scholar
  37. Russell, A. P., & Bauer, A. M. (2002). Underwood’s classification of the geckos: a 21st century appreciation. Bulletin of the British Museum (Natural History) Zoology, 68(2), 113–121.Google Scholar
  38. Samonds, K. E., Godfrey, L. R., Ali, J. R., Goodman, S. M., Vences, M., Sutherland, M. R., Irwin, M. T., & Krause, D. W. (2012). Spatial and temporal arrival patterns of Madagascar’s vertebrate fauna explained by distance, ocean currents, and ancestor type. Proceedings of the National Academy of Sciences of the USA, 109(14), 5352–5357.CrossRefPubMedCentralPubMedGoogle Scholar
  39. Schimmenti, G., & Jesu, R. (1996). Brookesia exarmata sp. n. (Reptilia, Chamaeleonidae): a new dwarf chameleon from the limestone outcrops of western Madagascar. Italian Journal of Zoology, 63, 193–197.CrossRefGoogle Scholar
  40. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  41. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis. Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedCentralPubMedGoogle Scholar
  42. Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.PubMedCentralPubMedGoogle Scholar
  43. Townsend, T. M., Vieites, D. R., Glaw, F., & Vences, M. (2009). Testing species-level diversification hypotheses in Madagascar: the case of microendemic Brookesia leaf chameleons. Systematic Biology, 58, 461–656.CrossRefGoogle Scholar
  44. Vences, M., Vieites, D. R., Glaw, F., Brinkmann, H., Kosuch, J., Veith, M., & Meyer, A. (2003). Multiple overseas dispersal in amphibians. Proceedings of the Royal Society B: Biological Sciences, 270, 2435–2442.Google Scholar
  45. Vences, M., Wollenberg, K. C., Vieites, D. R., & Lees, D. C. (2009). Madagascar as a modelregion of species diversification. Trends in Ecology and Evolution, 24, 456–465.Google Scholar
  46. 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 USA, 104, 19903–19907.CrossRefPubMedCentralPubMedGoogle Scholar
  47. 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 USA, 106, 8267–8272.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2014

Authors and Affiliations

  • Angelica Crottini
    • 1
    • 2
    Email author
  • D. James Harris
    • 1
  • Aurélien Miralles
    • 2
    • 3
  • Frank Glaw
    • 4
  • Richard K. B. Jenkins
    • 5
    • 6
  • J. Christian Randrianantoandro
    • 5
  • Aaron M. Bauer
    • 7
  • Miguel Vences
    • 2
  1. 1.CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do PortoVila do CondePortugal
  2. 2.Division of Evolutionary Biology, Zoological InstituteTechnical University of BraunschweigBraunschweigGermany
  3. 3.CNRS-UMR5175 CEFE, Centre d’Ecologie Fonctionelle et EvolutiveMontpellier CEDEX 5France
  4. 4.Zoologische Staatssammlung MünchenMunichGermany
  5. 5.Madagasikara VoakajyAntananarivoMadagascar
  6. 6.Durrell Institute of Conservation and Ecology, School of Anthropology and ConservationUniversity of KentCanterburyUK
  7. 7.Department of BiologyVillanova UniversityVillanovaUSA

Personalised recommendations