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Organisms Diversity & Evolution

, Volume 13, Issue 4, pp 605–620 | Cite as

Northern origin and diversification in the central lowlands? – Complex phylogeography and taxonomy of widespread day geckos (Phelsuma) from Madagascar

  • Philip-Sebastian Gehring
  • Frank Glaw
  • Marcelo Gehara
  • Fanomezana Mihaja Ratsoavina
  • Miguel VencesEmail author
Original Article

Abstract

Day geckos of the Phelsuma lineata group are widespread in Madagascar and have been historically split into numerous species and subspecies based almost exclusively on differences in coloration and body size. We apply phylogenetic and phylogeographic methods to examine the biogeography and taxonomy of these lizards, including explicit tests of various biogeographic predictions and based on a molecular data set covering much of the distribution ranges of all species and subspecies of P. lineata, P. dorsivittata, P. comorensis, P. hoeschi, P. kely, and P. pusilla in Madagascar (and the Comoros archipelago for P. comorensis). Sequences of the mitochondrial 16S rRNA and the nuclear RAG-1 gene fragment were determined from 376 samples, and a multigene mtDNA phylogeny of the species group was constructed for the main phylogroups identified in the 16S haplotype network. We used the 16S sequences to estimate the geographic location of the ancestor of each major mtDNA clade and to infer their demographic history using a variety of statistical tools. Our phylogeny separates the taxa analyzed into two well-supported major subclades mainly occurring in the north respectively east of the island. Mismatch distribution of samples together with rejection of neutrality, the results of Bayesian Skyline Plots analysis, and a star-like network suggests a recent demographic expansion for the P. l. lineata lineage into the eastern lowlands, while the highland (P. l. elanthana) and northern clades (P. dorsivittata and P. l. punctulata) show signatures of rather stable populations. A major genetic discontinuity observed coincided with a northern lowland stretch that separates mid-altitude rainforests in the north from those in the center and south. Our analysis points to numerous unsolved taxonomic problems in this group of geckos, especially in the small-sized taxa (P. hoeschi, P. kely, P. pusilla), and provides a basis for a future comprehensive taxonomic revision, which will require integrative analysis of molecular, morphological and chromatic data as well as careful examination of type specimens.

Keywords

Squamata, Gekkonidae Phelsuma lineata species group Biogeography Multigene mtDNA phylogeny 16S rRNA RAG-1 

Notes

Acknowledgements

We are grateful to a large number of friends, colleagues, and students who assisted during field work, in particular to Jason L. Brown, Jörn Köhler, James and Carol Patton, Emile Rajeriarison, Theo Rajoafiarison, Roger-Daniel Randrianiaina, and David R. Vieites. Hans-Peter Berghof, Angelica Crottini, Arne Hartig, Susanne Hauswaldt, Thomas Hofmann, Alexandra Lima, Maciej Pabijan, and Patrick Schönecker provided pictures and additional samples. Gabi Keunecke, Meike Kondermann, and Eva Saxinger provided crucial help in the laboratory. This work was carried under a collaboration accord between TU Braunschweig and the Université d’Antananarivo, Département de Biologie Animale. We are grateful to the Malagasy authorities for research and export permits. Financial support was provided by the Volkswagen Foundation and by the Deutsche Gesellschaft für Herpetologie und Terrarienkunde (DGHT) to PSG, FG, and MV.

Supplementary material

13127_2013_143_MOESM1_ESM.pdf (265 kb)
ESM 1 (PDF 265 kb)

References

  1. Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19, 716–723.CrossRefGoogle Scholar
  2. Althoff, D. M., & Pellmyr, O. (2002). Examining genetic structure in a bogus yucca moth: a sequential approach to phylogeography. Evolution, 56, 1632–1643.PubMedGoogle Scholar
  3. Anderson, S., & Marcus, L. F. (1992). Aerography of Australian tetrapods. Australian Journal of Zoology, 40, 627–651.CrossRefGoogle Scholar
  4. Austin, J. J., Arnold, E. N., & Jones, C. G. (2004). Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene islands. Molecular Phylogenetics and Evolution, 31, 102–109.CrossRefGoogle Scholar
  5. Bandelt, H.-J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.PubMedCrossRefGoogle Scholar
  6. Bauer, A., Glaw, F., Gehring, P.-S., & Vences, M. (2011). New species of Blaesodactylus (Squamata: Gekkonidae) from Ankarafantsika National Park in north-western Madagascar. Zootaxa, 2942, 57–68.Google Scholar
  7. Berghof, H. P., & Trautmann, G. (2009). Eine neue Art der Gattung Phelsuma Gray, 1825 (Sauria: Gekkonidae) von der Ostküste Madagaskars. Sauria, 31, 5–14.Google Scholar
  8. Böhm, M., et al. (2013). The conservation status of the world’s reptiles. Biological Conservation, 157, 372–385 (261 authors).CrossRefGoogle Scholar
  9. Bond, W., Silander, J. A., Jr., Ranaivonasy, J., & Ratsirarson, J. (2008). The antiquity of Madagascar’s grasslands and the rise of C4 grassy biomes. Journal of Biogeography, 35, 1743–1758.CrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. Brandley, M. C., Schmitz, A., & Reeder, T. W. (2005). Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology, 54, 373–390.PubMedCrossRefGoogle Scholar
  12. Bruford, M. W., Hanotte, O., Brookfield, J. F. Y., & Burke, T. (1992). Singlelocus 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
  13. Camargo, A., Sinervo, B., & Sites, J. W., Jr. (2010). Lizards as model organisms for linking phylogeographic and speciation studies. Molecular Ecology, 19, 3250–3270.PubMedCrossRefGoogle Scholar
  14. Chiari, Y., van der Meijden, A., Madsen, O., Vences, M., & Meyer, A. (2009). Base composition, selection, and phylogenetic significance of indels in the recombination activating gene-1 in vertebrates. Frontiers in Zoology, 6, article 32.Google Scholar
  15. Clark, P. U., Dyke, A. S., Shakun, J. D., Carlson, A. E., Clark, J., Wohlfarth, B., et al. (2009). The last glacial maximum. Science, 325, 710–714.PubMedCrossRefGoogle Scholar
  16. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.PubMedCrossRefGoogle Scholar
  17. Delport, W., Poon, A. F., Frost, S. D. W., & Pond, S. L. K. (2010). Pond Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics, 26, 2455–2457.PubMedCrossRefGoogle Scholar
  18. Drummond, A. J., Rambaut, A., Shapiro, B., & Pybus, O. G. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185–1192.PubMedCrossRefGoogle Scholar
  19. Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.PubMedCrossRefGoogle Scholar
  20. Endler, J. A. (1977). Geographic variation, speciation, and clines. Princeton University Press.Google Scholar
  21. Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.PubMedCrossRefGoogle Scholar
  22. Fu, Y. X. (1997). Statistical tests of neutrality against population growth, hitchhiking and background selection. Genetics, 147, 915–925.PubMedGoogle Scholar
  23. Gehring, P.-S., Crottini, A., Glaw, F., Hauswaldt, S., & Ratsoavina, F. M. (2010). Notes on the natural history, distribution and malformations of day geckos (Phelsuma) from Madagascar. Herpetology Notes, 3, 321–327.Google Scholar
  24. Gehring, P.-S., Ratsoavina, F. M., Vences, M., & Glaw, F. (2011). Calumma vohibola, a new chameleon species (Squamata: Chamaeleonidae) from the littoral forests of eastern Madagascar. African Journal of Herpetology, 60, 130–154.CrossRefGoogle Scholar
  25. Gehring, P.-S., Tolley, K., Eckhardt, F. S., Townsend, T. M., Ziegler, T., Ratsoavina, F. M., et al. (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.PubMedCrossRefGoogle Scholar
  26. Glaw, F., & Vences, M. (2007). A field guide to the amphibians and reptiles of Madagascar (3rd ed.). Köln (Cologne): Vences & Glaw Verlag. 496 pp.Google Scholar
  27. Glaw, F., Köhler, J., Townsend, T. M., & Vences, M. (2012). Rivaling the world’s smallest reptiles: Discovery of miniaturized and microendemic new species of leaf chameleons (Brookesia) from northern Madagascar. PLoS ONE, 7, doi: 10.1371/journal.pone.0031314.
  28. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.PubMedCrossRefGoogle Scholar
  29. Hallmann, G., Krüger, J., & Trautmann, G. (Eds.). (2008). Faszinierende Taggeckos. Die Gattung Phelsuma (2. Auflage). Münster: Natur und Tier-Verlag. 253 pp.Google Scholar
  30. Harmon, L. J., Melville, J., Larson, A., & Losos, J. B. (2008). The role of geography and ecological opportunity in the diversification of Day Geckos (Phelsuma). Systematic Biology, 57, 562–573.PubMedCrossRefGoogle Scholar
  31. Harpending, H. C. (1994). Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591–600.PubMedGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. Knowles, L. L. (2009). Statistical phylogeography. Annual Review of Ecology, Evolution, and Systematics, 40, 593–612.CrossRefGoogle Scholar
  34. Kratysberg, Y., Schwartz, M., & Brown, T. A. (2004). Recombination of human mitochondrial DNA. Science, 304, 981.CrossRefGoogle Scholar
  35. Krüger, J. (1996). Zur Nomenklatur der lineata-Gruppe in der Gattung Phelsuma (Reptilia: Sauria: Gekkonidae). Sauria, 18, 37–42.Google Scholar
  36. 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
  37. Lemmon, A., & Lemmon, E. (2008). A likelihood framework for estimating phylogeographic history on a continuous landscape. Systematic Biology, 57, 544–561.PubMedCrossRefGoogle Scholar
  38. Librado, P., & Rozas, J. (2009). DNASP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.PubMedCrossRefGoogle Scholar
  39. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D., & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics, 26, 2462–2463.PubMedCrossRefGoogle Scholar
  40. Maruyama, T., & Birky, C. W., Jr. (1991). Effects of periodic selection on gene diversity in organelle genomes and other systems without recombination. Genetics, 127, 449–451.PubMedGoogle Scholar
  41. Meier, H. (1989). Eine neue Form aus der lineata-Gruppe der Gattung Phelsuma auf Madagaskar. Salamandra, 25, 230–236.Google Scholar
  42. Moritz, C., Patton, J. L., Schneider, C. J., & Smith, T. B. (2000). Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology and Systematics, 31, 533–563.CrossRefGoogle Scholar
  43. 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
  44. 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, doi: 10.1371/journal.pone.0034506
  45. Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondavony, D., Guschanski, K., et al. (2007). The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution, 43, 309–327.PubMedCrossRefGoogle Scholar
  46. Palumbi, S., Martin, A., Ramano, S., McMillan, W. O., Stice, L., & Grabowski, G. (1991). The simple fool’s guide to PCR, version 2. Honolulu, Hawaii: University of Hawaii Zoology Department. 46 pp.Google Scholar
  47. Pond, S. L. K., & Frost, S. D. W. (2005). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics, 21, 2531–2533.PubMedCrossRefGoogle Scholar
  48. Pond, S. L. K., Posada, D., Gravenor, M. B., Woelk, C. H., & Frost, S. D. W. (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Molecular Biology and Evolution, 23, 1891–1901.CrossRefGoogle Scholar
  49. Posada, D. (2008). JModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.PubMedCrossRefGoogle Scholar
  50. Posada, D., & Crandall, K. A. (2001). Selecting the best-fit model of nucleotide substitution. Systematic Biology, 50, 580–601.PubMedCrossRefGoogle Scholar
  51. Rambaut, A., & Drummond, A. J. (2009). Tracer v1.5 Available at http://beast.bio.ed.ac.uk/Tracer
  52. Ramos-Onsins, R., & Rozas, R. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092–2100.PubMedCrossRefGoogle Scholar
  53. Ratsoavina, F. M., Louis, E. E., Jr., Crottini, A., Randrianiaina, R. D., Glaw, F., & Vences, M. (2011). A new leaf tailed gecko species from northern Madagascar with a preliminary assessment of molecular and morphological variability in the Uroplatus ebenaui group. Zootaxa, 3022, 39–57.Google Scholar
  54. Raxworthy, C. J., & Nussbaum, R. A. (1995). Systematics, speciation and biogeography of the dwarf chameleons (Brookesia, Reptilia, Squamata, Chamaeleontidae) of northern Madagascar. Journal of Zoology, 235, 525–558.CrossRefGoogle Scholar
  55. Raxworthy, C. J., Ingram, C. M., Rabibisoa, N., & Pearson, R. G. (2007). Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using Day Geckos (Phelsuma) from Madagascar. Systematic Biology, 56, 907–923.PubMedCrossRefGoogle Scholar
  56. 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.PubMedCrossRefGoogle Scholar
  57. Rocha, S., Rösler, H., Gehring, P.-S., Glaw, F., Posada, D., Harris, D. J., et al. (2010). Phylogenetic systematics of day geckos, genus Phelsuma, based on molecular and morphological data (Squamata: Gekkonidae). Zootaxa, 2429, 1–28.Google Scholar
  58. Rogers, A. R., & Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.PubMedGoogle Scholar
  59. Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.PubMedCrossRefGoogle Scholar
  60. Schatz, G. E., Lowry, P. P., II, & Ramisamihantanirina, A. (1998). Takhtajania perrieri rediscovered. Nature, 391, 133–134.CrossRefGoogle Scholar
  61. Schönecker, P. (2008). Terralog Vol. 12: geckos of Madagascar, the Seychelles, Comoros and Mascarene Islands – Geckos Madagaskars, der Seychellen, Komoren und Maskarenen. Edition Chimaira, Frankfurt am Main, 144 p.Google Scholar
  62. Simonsen, K., Churchill, G., & Aquadro, C. (1995). Properties of statistical tests of neutrality for DNA polymorphism data. Genetics, 141, 413–429.PubMedGoogle Scholar
  63. Slatkin, M., & Hudson, R. R. (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555–562.PubMedGoogle Scholar
  64. Stephens, M., & Scheet, P. (2005). Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. American Journal of Human Genetics, 76, 449–462.PubMedCrossRefGoogle Scholar
  65. 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.PubMedCrossRefGoogle Scholar
  66. Swofford, D. L. (2002). PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
  67. Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.PubMedGoogle Scholar
  68. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedCrossRefGoogle Scholar
  69. Toju, H., & Sota, T. (2006). Phylogeography and the geographic cline in the armament of a seed-predatory weevil: effects of historical events vs. natural selection from the host plant. Molecular Ecology, 15, 4161–4173.PubMedCrossRefGoogle Scholar
  70. Vences, M., Wollenberg, K. C., Vieites, D. R., & Lees, D. C. (2009). Madagascar as a model region of species diversification. Trends in Ecology & Evolution, 24, 456–465.CrossRefGoogle Scholar
  71. 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 U.S.A., 106, 8267–8272.CrossRefGoogle Scholar
  72. Wilmé, L., Goodman, S. M., & Ganzhorn, J. U. (2006). Biogeographic evolution of Madagascar’s microendemic biota. Science, 312, 1063–1065.PubMedCrossRefGoogle Scholar
  73. 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.PubMedCrossRefGoogle Scholar
  74. Yoder, A. D., & Heckman, K. (2006). Mouse lemur phylogeography revises a model of ecogeographic constraint in Madagascar. In Primate biogeography: Progress and prospects. Fleagle, J., Lehman, S. M., (eds), pp. 255–268, Kluwer.Google Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2013

Authors and Affiliations

  • Philip-Sebastian Gehring
    • 1
  • Frank Glaw
    • 2
  • Marcelo Gehara
    • 1
  • Fanomezana Mihaja Ratsoavina
    • 1
    • 3
  • Miguel Vences
    • 1
    Email author
  1. 1.Division of Evolutionary Biology, Zoological InstituteTechnical University of BraunschweigBraunschweigGermany
  2. 2.Zoologische Staatssammlung MünchenMünchenGermany
  3. 3.Département de Biologie AnimaleUniversité d’AntananarivoAntananarivo 101Madagascar

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