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Organisms Diversity & Evolution

, Volume 16, Issue 1, pp 289–298 | Cite as

Resurrection of the Comoran fish scale gecko Geckolepis humbloti Vaillant, 1887 reveals a disjunct distribution caused by natural overseas dispersal

  • Oliver HawlitschekEmail author
  • Mark D. Scherz
  • Nicolas Straube
  • Frank Glaw
Original Article

Abstract

Fish scale geckos (Geckolepis) are taxonomically poorly resolved, mainly because of the difficulty of applying standard morphological characters to diagnose taxa. Three species, Geckolepis maculata, G. polylepis, and G. typica, are currently recognized from Madagascar and the Comoro Islands. Molecular studies suggested a number of operational taxonomical units within the G. maculata complex, but none of these has been formally described. The Comoran population was described as Geckolepis humbloti Vaillant 1887 but later synonymized. Prior to our study, no genetic data and little other information were available for this taxon. We revised the status of G. humbloti using molecular genetics, external morphology, and osteological characters retrieved from 3D skeletal models created using micro-computed tomography (micro-CT). Our results demonstrate that G. humbloti represents a genetic lineage strongly distinct from all other Geckolepis species. It is furthermore distinguished by a combination of external morphological characters and probably by osteology. We therefore resurrect G. humbloti Vaillant, 1887 from synonymy with G. maculata. Remarkably, this lineage is not restricted to the Comoros: A specimen from Tsingy de Bemaraha in western Madagascar falls as a closely related sister lineage to all Comoran Geckolepis in our molecular phylogenetic analysis and is osteologically almost identical with a specimen from the type locality Grand Comoro. We therefore include it in G. humbloti. The phylogenetic topology and the intraspecific genetic divergences suggest that the Comoros were colonized naturally from western Madagascar by overseas dispersal. G. humbloti is not considered as threatened, but its presence is indicative of natural or near-natural habitats.

Keywords

Biogeography Madagascar Mayotte Reptiles Taxonomy Tsingy de Bemaraha 

Notes

Acknowledgments

For their participation and invaluable help in the field surveys, we are grateful to Johannes Berger, Boris Brückmann, Bastian Brenzinger, Maoulida ‘Kamal’ Badroudine, Hadidja Sinane, Sheikh Moussa, Hugh Doulton, Katie Green, Ishaka Said, Amelaid Houmadi, and other members of the staff of Bristol Conservation and Science Foundation’s project in the Comoros (www.bscf.org.uk/comoros), Michel Charpentier from the Naturalistes de Mayotte, and Danny Laybourne, Guillaume Viscardi, and the other members of the DAF Mayotte. We are also grateful to Ivan Ineich (MNHN Paris), for granting access to the herpetological collection. Thanks are also due to Cynthia Wang and Bernhard Ruthensteiner for their help with micro-CT scans, Ella Z. Lattenkamp for her assistance with measurements and meristics, and Michael Franzen for general support. Authorities at Moroni (Comoros) and Mamoudzou (Mayotte) are acknowledged for the collection and export permits. Finally, we thank Michael Balke, Munich, for providing lab infrastructure, the EMBL team for handling the GenBank entries, and the editor, two anonymous reviewers, and Gunther Köhler, Frankfurt, for their helpful comments, which greatly improved this paper.

Compliance with ethical standards

Funding

The research was financially supported by the Mohamed bin Zayed Species Conservation Fund (project 0925157) to FG and OH (http://www.mbzspeciesconservation.org/), by DAAD grant D/09/49634 to OH (http://www.daad.de/en/), and the “Deutsche Forschungsgemeinschaft” DFG GL 314/1 to FG and BA2152/7-1 to Michael Balke (http://www.dfg.de/en/index.jsp). The “Freunde der Zoologischen Staatssammlung München” (http://www.zsm.mwn.de/freunde/) and the EES funding program of the University of Munich (http://www.eeslmu.de/eeswiki/Main_Page) provided additional financial support.

Conflict of interest

The authors declare that no conflict of interest exists.

Ethical approval

All animal handling was conducted according to guidelines approved by an ethics committee.

Supplementary material

13127_2015_255_MOESM1_ESM.xlsx (15 kb)
A 1 Table with individual morphological data and locality records for all specimens studied. (XLSX 15 kb)
13127_2015_255_MOESM2_ESM.pdf (14.7 mb)
A 2 Interactive 3D models of the skulls of two scanned individuals of Geckolepis humbloti. ZSM 80/2010, collected from the type locality, Grand Comoro. ZSM 81/2006, collected from the Tsingy de Bemaraha. For full body models, see Appendix A3. Models can be viewed in Adobe Reader 9 or above, or Adobe Acrobat Pro X or above. Click the image to activate it. (PDF 15033 kb)
13127_2015_255_MOESM3_ESM.pdf (16.8 mb)
A 3 Interactive 3D models of the full skeletons of two scanned individuals of Geckolepis humbloti. ZSM 80/2010 (Grand Comoro) and ZSM 81/2006 (Tsingy de Bemaraha, western Madagascar. For skull models, see Appendix A2. Models can be viewed in Adobe Reader 9 or above, or Adobe Acrobat Pro X or above. Click the image to activate it. (PDF 17238 kb)

References

  1. Angel, F. (1942). Les lézards de Madagascar. Mémoires de l’Académie Malgache, 36, 1–193.Google Scholar
  2. Battistini, R., & Cremers, G. (1972). Geomorphology and vegetation of Îles Glorieuses. Atoll Research Bulletin, 159, 1–27.CrossRefGoogle Scholar
  3. Boettger, O. (1893). Katalog der Reptilien-Sammlung im Museum der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt am Main. I. Teil (Rhynchocephalen, Schildkröten, Krokodile, Eidechsen, Chamäleons). Frankfurt: Gebrüder Knauer.Google Scholar
  4. Daza, J. D., Abdala, V., Thomas, R., & Bauer, A. M. (2008). Skull anatomy of the miniaturized gecko Sphaerodactylus roosevelti (Squamata: Gekkota). Journal of Morphology, 269, 1340–1346.PubMedGoogle Scholar
  5. Daza, J. D., Aurich, J., & Bauer, A. M. (2012). Anatomy of an enigma: an osteological investigation of the Namibian festive gecko (Narudasia festiva: Gekkonidae: Gekkota). Acta Zoologica, 93, 465–486.CrossRefGoogle Scholar
  6. Gamble, T., Greenbaum, E., Jackman, T. R., Russell, A. P., & Bauer, A. M. (2012). Repeated origin and loss of adhesive toepads in geckos. PLoS ONE, 7(6), e39429.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Goodman, S. M., & Benstead, J. P. (2003). The Natural History of Madagascar. University of Chicago Press. 1709 pp.Google Scholar
  8. Grandidier, A. (1867). Liste des reptiles nouveaux découverts, en 1866, sur la côte sud-ouest de Madagascar. Revue et Magazine de Zoologie, 19(2), 232–234.Google Scholar
  9. Greenbaum, E., Bauer, A. M., Jackman, T. R., Vences, M., & Glaw, F. (2007). A phylogeny of the enigmatic Madagascan geckos of the genus Uroplatus (Squamata: Gekkonidae). Zootaxa, 1493, 41–51.Google Scholar
  10. Hawlitschek, O., & Glaw, F. (2013). The complex colonization history of nocturnal geckos (Paroedura) in the Comoros Archipelago. Zoologica Scripta, 42, 135–150.CrossRefGoogle Scholar
  11. Hawlitschek, O., & Glaw, F. (2014). Determinant species of reptiles and amphibians for the delimitation of ZNIEFF zones in Mayotte. Expert report with field surveys for the delimitation of ‘Zones naturelles d’intérêt écologique, faunistique et floristique’ (ZNIEFF, natural regions of ecological, faunal, and floral importance) in Mayotte. Mayotte, France: Expert report on behalf of the prefecture of Mayotte (French overseas department), Department for Management of Environment, Landscape, and Housing (DEAL). 43 pp.Google Scholar
  12. Hawlitschek, O., Brückmann, B., Berger, J., Green, K., & Glaw, F. (2011). Integrating field surveys and remote sensing data to study distribution, habitat use and conservation status of the herpetofauna of the Comoro Islands. Zookeys, 144, 21–79.CrossRefPubMedGoogle Scholar
  13. Hawlitschek, O., Nagy, Z. T., & Glaw, F. (2012). Island evolution and systematic revision of Comoran snakes: why and when subspecies still make sense. PLoS ONE, 7(8), e42970.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hawlitschek, O., Nagy, Z. T., Berger, J., & Glaw, F. (2013). Reliable DNA barcoding performance proved for species and island populations of Comoran squamate reptiles. PLoS ONE, 8(9), e73368.CrossRefPubMedPubMedCentralGoogle Scholar
  15. IUCN (2001). IUCN Red List categories and criteria (version 3.1). IUCN Species Survival Commission. Gland: IUCN.Google Scholar
  16. IUCN France, & MNHN (2014). The Red List of threatened species in France. Chapter reptiles and amphibians of Mayotte. Edited by Hawlitschek, O., Glaw, F., Gigot, G. & Kirchner, F. Paris, France.Google Scholar
  17. Jackman, T. R., Bauer, A. M., Greenbaum, E., Glaw, F., & Vences, M. (2008). Molecular phylogenetic relationships among species of the Malagasy-Comoran gecko genus Paroedura (Squamata: Gekkonidae). Molecular Phylogenetics and Evolution, 46, 74–81.CrossRefPubMedGoogle Scholar
  18. Jerez, A., Mangione, S., & Abdala, V. (2010). Occurrence and distribution of sesamoid bones in squamates: a comparative approach. Acta Zoologica, 91, 295–305.Google Scholar
  19. Jono, T. (2015). Feeding behavior on tree sap and planthopper-derived honeydew by a fish-scale gecko (Geckolepis sp.) in a dry forest of Madagascar. Current Herpetology, 34(1), 85–88.CrossRefGoogle Scholar
  20. Köhler, G., Diethert, H. H., Nussbaum, R. A., & Raxworthy, C. J. (2009). A revision of the fish scale geckos, genus Geckolepis Grandidier (Squamata, Gekkonidae) from Madagascar and the Comoros. Herpetologica, 65, 419–435.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Louette, M., Meirte, D., & Jocque, R. (2004). La faune terrestre de l’archipel des Comores. MRAC, Tervuren, Belgium. Afrotropical Zoology, 293, 456.Google Scholar
  23. Maddison, W. P., & Maddison, D. R. (2015). Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org.
  24. Methuen, P. A., & Hewitt, J. (1913). On a collection of reptiles from Madagascar made during the year 1911. Annals of the Transvaal Museum, 3, 183–193.Google Scholar
  25. Miralles, A., Vasconcelos, R., Perera, A., Harris, D. J., & Carranza, S. (2011). An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). Zoologica Scripta, 40, 16–44.CrossRefGoogle Scholar
  26. Mocquard, F. (1909). Synopsis des familles, genres et espèces des reptiles écailleux et des batraciens de Madagascar. Nouvelles Archives du Museum National d’Histoire Naturelle, Paris, 1(5), 1–108.Google 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. Peters, W. (1880). Über die von Hrn J. M. Hildebrandt auf Nossi-Bé und Madagascar gasammelten Säugethiere und Amphibien. Monatsberichte der Königlich Preussischen Akademie der Wissenschaften zu Berlin, 1880, 508–511.Google Scholar
  29. Ratsoavina, F. M., Vences, M., & Louis, E. E., Jr. (2012). Phylogeny and phylogeography of the Malagasy leaf-tailed geckos in the Uroplatus ebenaui group. African Journal of Herpetology, 61, 143–158.CrossRefGoogle Scholar
  30. Ratsoavina, F. M., Ranjanaharisoa, F. A., Glaw, F., Raselimanana, A., Miralles, A., & Vences, M. (2015). A new leaf-tailed gecko of the Uroplatus ebenaui group (Squamata: Gekkonidae) from Madagascar’s central eastern rainforests. Zootaxa, 4006, 143–160.CrossRefPubMedGoogle Scholar
  31. Raxworthy, C. J., Pearson, R. G., Zimkus, B. M., Reddy, S., Deo, A. J., Nussbaum, R. A., & Ingram, C. M. (2008). Continental speciation in the tropics: contrasting biogeographic patterns of divergence in the Uroplatus leaf-tailed gecko radiation of Madagascar. Journal of Zoology, 275, 423–440.CrossRefGoogle Scholar
  32. Rocha, S., Carretero, M. A., Vences, M., Glaw, F., & Harris, D. J. (2006). Deciphering patterns of transoceanic dispersal: the evolutionary origin and biogeography of coastal lizards (Cryptoblepharus) in the Western Indian Ocean region. Journal of Biogeography, 33, 13–22.CrossRefGoogle Scholar
  33. Rocha, S., Posada, D., Carretero, M. A., & Harris, D. J. (2007). Phylogenetic affinities of Comoroan and East African day geckos (genus Phelsuma): multiple natural colonisations, introductions and island radiations. Molecular Phylogenetics and Evolution, 43, 685–692.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. Romer, A. S. (1956). The Osteology of the Reptiles. Chicago: The University of Chicago Press.Google Scholar
  36. Rosenberg, N. A. (2007). Statistical tests for taxonomic distinctiveness from observations of monophyly. Evolution, 61, 317–323.CrossRefPubMedGoogle Scholar
  37. Ross, H. A., Murugan, S., & Li, W. L. S. (2008). Testing the reliability of genetic methods of species identification via simulation. Systematic Biology, 57, 216–230.CrossRefPubMedGoogle Scholar
  38. Russell, A. P., & Bauer, A. M. (2008). The appendicular locomotor apparatus of Sphenodon and normal-limbed squamates. In C. Gans, A. S. Gaunt, & K. Adler (Eds.), The skull and Appendicular locomotor apparatus of Lepidosauria. Biology of the Reptilia (Vol. 21, pp. 1–465). Ithaca: Society for the Study of Amphibians and Reptiles.Google Scholar
  39. Schubert, C., Steffen, T., & Christophers, E. (1990). Weitere Beobachtungen zur “dermolytischen Schreckhäutung” bei Geckolepis typica (Reptilia, Gekkonidae). Zoologischer Anzeiger, 224, 175–192.Google Scholar
  40. Silvestro, M. (2012). raxmlGUI: a graphical front-end for RAxML. Organisms, Diversity and Evolution, 12, 335–337.CrossRefGoogle Scholar
  41. Stamatakis, A (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014: open access.Google Scholar
  42. Stamatakis, A. (2015). The RAxML v8.2.X Manual. Heidelberg: Heidelberg Institute for Theoretical Studies.Google Scholar
  43. Vaillant, L. (1887). Matériaux pour servir l’histoire herpétologique des Iles Comores. Bulletin de la Société Philomathique de Paris, 11, 131–136.Google Scholar
  44. Wang C., Scherz M. D., Montfort L., Hawlitschek O. (2015). Complementary herpetological surveys to complete the ZNIEFF database of Mayotte: results. Mayotte, France: Expert report on behalf of the prefecture of Mayotte (French overseas department), Department for Management of Environment, Landscape, and Housing (DEAL). 31 pp.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2015

Authors and Affiliations

  • Oliver Hawlitschek
    • 1
    • 2
    Email author
  • Mark D. Scherz
    • 2
  • Nicolas Straube
    • 2
  • Frank Glaw
    • 2
  1. 1.Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra)BarcelonaSpain
  2. 2.Zoologische Staatssammlung München (ZSM-SNSB)MunichGermany

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