Open Access Open Access  Restricted Access Subscription or Fee Access

Applying n-dimensional hypervolumes for species delimitation: unexpected molecular, morphological, and ecological diversity in the Leaf-Toed Gecko Phyllodactylus reissii Peters, 1862 (Squamata: Phyllodactylidae) from northern Peru

CLAUDIA KOCH, MORRIS FLECKS, PABLO J. VENEGAS, PATRICK BIALKE, SEBASTIAN VALVERDE, DENNIS RÖDDER

Abstract


An integrative taxonomic approach based on morphology, molecular analyses, and climatic niche modeling was used to uncover cryptic diversity in the phyllodactylid gecko species Phyllodactylus reissii. At least three distinct species could be identified among the examined specimens from southern Ecuador and northern Peru. Phyllodactylus magister, described by Noble (1924) from arid Andean valleys of the Chinchipe and Marañón rivers in the Peruvian Department of Cajamarca and synonymized with P. reissii by Dixon & Huey (1970) is elevated from synonymy and a detailed redescription is provided. A new species of the genus Phyllodactylus from the Andean dry forest of the southern Marañón valley is identified and described herein. Phyllodactylus pachamama sp. nov. is differentiated from other South American congeners on the basis of mtDNA sequence divergence, morphological characters, and differences in the realized climatic niche. At least in Peru, P. reissii seems to primarily inhabit the northern coastal region west of the Andes, while the inter-Andean area along the Río Marañón and its tributaries seems to be inhabited mostly by other species of the genus, which are endemic to this area. The Andean valleys are underestimated in terms of biodiversity and lack thorough investigation and conservation actions.

 


Keywords


Reptilia, new Phyllodactylus, Gekkota, Andes, Marañón valley, realized niche comparison, morphology, species delimitation, Phyllodactylus magister, phylogenetic relationships, molecular analysis, 12S rRNA, 16S rRNA

Full Text:

PDF (4MB)

References


Aguilar, C., Wood, P., Cusi, J.C., Guzman, A., Huari, F., Lundberg, M., Mortensen, E., Ramirez, C., Robles, D., Suarez, J., Ticona, A., Vargas, V., Venegas, P.J. & Sites, J. (2013) Integrative taxonomy and preliminary assessment of species limits in the Liolaemus walkeri complex (Squamata, Liolaemidae) with descriptions of three new species from Peru. ZooKeys, 364, 47–91.

http://dx.doi.org/10.3897/zookeys.364.6109

Aurich, J., Koch, C. & Böhme, W. (2011) Ecology of a unique gecko assemblage (Phyllodactylidae: Squamata) from northern Peru. Northwestern Journal of Zoology, 7 (2), 310–317.

Aurich, J., Koch, C. & Böhme, W. (2015) Reproduction of a gecko assemblage (Squamata: Phyllodactylidae) in the Marañon Region (Peru) and comments on the largest gekkonid in the New World. Phyllomedusa, 14 (1), 53–62.
http://dx.doi.org/10.11606/issn.2316-9079.v14i1p53-62

Barata, M., Perera, A., Martínez-Freiría, F. & Harris, D.H. (2012) Cryptic diversity within the Moroccan endemic day geckos Quedenfeldtia (Squamata: Gekkonidae): a multidisciplinary approach using genetic, morphological and ecological data. Biological Journal of the Linnean Society, 106 (4), 828–850.
http://dx.doi.org/10.1111/j.1095-8312.2012.01903.x

Bergmann, P.J. & Russell, A.P. (2007) Systematics and biogeography of the widespread Neotropical gekkonid genus Thecadactylus (Squamata), with the description of a new cryptic species. Zoological Journal of the Linnean Society, 149, 339–370.
http://dx.doi.org/10.1111/j.1096-3642.2007.00251.x

Bickford, D., Lohman, D.J., Navjot, S.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2006) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22, 148–155.
http://dx.doi.org/10.1016/j.tree.2006.11.004

Blair, C., Méndez de la Cruz, F.R., Law, C. & Murphy, R.W. (2015) Molecular phylogenetics and species delimitation of leaf-toed geckos (Phyllodactylidae: Phyllodactylus) throughout the Mexican tropical dry forest. Molecular Phylogenetics and Evolution, 84, 254–265.
http://dx.doi.org/10.1016/j.ympev.2015.01.003

Blair, C., Méndez de la Cruz, F.R., Ngo, A., Lindell, J., Lathrop, A. & Murphy, R.W. (2009) Molecular phylogenetics and taxonomy of leaf-toed geckos (Phyllodactylidae: Phyllodactylus) inhabiting the peninsula of Baja California. Zootaxa, 2027, 28–42.

Blonder, B., Lamanna C., Violle C. & Enquist, B.J. (2014) The n-dimesional hypervolume. Global Ecology and Biogeography, 23, 595–609.
http://dx.doi.org/10.1111/geb.12146

Bridgewater, S., Pennington, R.T., Reynel, C.A., Daza, A. & Pennington, T.D. (2003) A preliminary floristic and phytogeographic analysis of the woody flora of seasonally dry forests in northern Peru. Candollea, 58, 129–141.

Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.
http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334

Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
http://dx.doi.org/10.1111/j.1095-8312.2005.00503.x

Domingos, F.M., Bosque, R.J., Cassimiro, J., Colli, G.R., Rodrigues, M.T., Santos, M.G. & Beheregaray, L.B. (2014) Out of the deep: cryptic speciation in a Neotropical gecko (Squamata, Phyllodactylidae) revealed by species delimitation methods. Molecular Phylogenetics and Evolution, 80, 113–124.
http://dx.doi.org/10.1016/j.ympev.2014.07.022

Dixon, J.R. (1964) The systematics and distribution of lizards of the genus Phyllodactylus in North and Central America. New Mexico State University Research Center Scientific Bulletin, 64, 1–139.

Dixon, J.R. & Huey, R.B. (1970) Systematics of the lizards of the gekkonid genus Phyllodactylus of mainland South America. Los Angeles County Museum Contributions in Science, 192, 1–78.

Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.
http://dx.doi.org/10.1093/nar/gkh340

Finer, M. & Jenkins, C.N. (2012) Proliferation of Hydroelectric Dams in the Andean Amazon and Implications for Andes–Amazon Connectivity. PLoS ONE, 7 (4), e35126.
http://dx.doi.org/10.1371/journal.pone.0035126

Fouquet, A., Loebmann, D., Castroviejo-Fisher, S., Padial, J.M., Orrico, V.G.D., Lyra, M.L., Joventino Roberto, I., Kok, P.J.R., Haddad, C.F.B. & Rodrigues, M.T. (2012) From Amazonia to the Atlantic forest: Molecular phylogeny of Phyzelaphryninae frogs reveals unexpected diversity and a striking biogeographic pattern emphasizing conservation challenges. Molecular Phylogenetics and Evolution, 65, 547–561.
http://dx.doi.org/10.1016/j.ympev.2012.07.012

Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology, 62, 707–724.

http://dx.doi.org/10.1093/sysbio/syt033

Funk, W.C., Caminer, M. & Ron, S.R. (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society of London B, 279 (1734), 1806–1814.
http://dx.doi.org/10.1098/rspb.2011.1653

Gamble, T., Colli, G.R., Rodrigues, M.T., Werneck, F.P. & Simons, A.M. (2012) Phylogeny and cryptic diversity in geckos (Phyllopezus; Phyllodactylidae; Gekkota) from South America’s open biomes. Molecular Phylogenetics and Evolution, 62 (3), 943–953.
http://dx.doi.org/10.1016/j.ympev.2011.11.033

Grismer, L.L., Wood, Jr, P.L., Anuar, S., Muin, M.A., Quah, E.S.H., Mcguire, J.A., Brown, R.M., Van Tri, N. & Thai, P.H. (2013) Integrative taxonomy uncovers high levels of cryptic species diversity in Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) and the description of a new species from Peninsular Malaysia. Zoological Journal of the Linnean Society, 169, 849–880.
http://dx.doi.org/10.1111/zoj.12064

Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.
http://dx.doi.org/10.1002/joc.1276

Hoogmoed, M.S. (1989) Introduced geckos in Puerto Ayora, Santa Cruz, with remarks on other areas. Noticias de Galápagos, 47, 12–16.

IUCN & UNEP-WCMC (2016) The World Database on Protected Areas (WDPA) [On-line]. UK: UNEP-WCMC, Cambridge. Available from: www.protectedplanet.net (accessed 4 April 2016)

Katoh, K., Asimenos, G. & Toh, H. (2009) Multiple Alignment of DNA Sequences with MAFFT. Methods in Molecular Biology, 537, 39–64.
http://dx.doi.org/10.1007/978-1-59745-251-9_3

Koch, C. & Beraún, A.M. (2011) Squamata, Phyllodactylidae, Phyllodactylus thompsoni Venegas, Townsend, Koch and Böhme 2008 and Phyllodactylus delsolari Venegas, Townsend, Koch and Böhme 2008: Latitudinal and altitudinal distribution extension and geographic distribution map. Check List, 7 (3), 272–275.

Koch, C., Venegas, P.J. & Böhme, W. (2006) A remarkable discovery: Description of a big-growing new gecko (Squamata: Gekkonidae: Phyllopezus) from northwestern Peru. Salamandra, 42 (2/3), 145–150.

Koch, C., Venegas, P.J. & Böhme, W. (2015) Three new endemic species of Epictia Gray, 1845 (Serpentes: Leptotyphlopidae) from the dry forest of northwestern Peru. Zootaxa, 3964 (2), 228–244.
http://dx.doi.org/10.11646/zootaxa.3964.2.4

Koch, C., Venegas, P.J., Garcia-Bravo, A. & Böhme, W. (2011) A new bush anole (Iguanidae: Polychrotinae: Polychrus) from the upper Marañón basin, Peru, with a redescription of Polychrus peruvianus (Noble, 1924) and additional information on P. gutturosus Berthold, 1845. Zookeys, 141, 79–107.
http://dx.doi.org/10.3897/zookeys.141.1678

Koch, C., Venegas, P.J., Rödder, D., Flecks, M. & Böhme, W. (2013) Two new endemic species of Ameiva (Squamata: Teiidae) from the dry forest of northwestern Peru and additional information on Ameiva concolor Ruthven, 1924. Zootaxa, 3745 (2), 263–295.
http://dx.doi.org/10.11646/zootaxa.3745.2.6

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 & Evolution, 13, 87–95.
http://dx.doi.org/10.1007/s13127-012-0098-y

Makhubo, B.G., Tolley, K.A. & Bates, M.F. (2015) Molecular phylogeny of the Afroedura nivaria (Reptilia: Gekkonidae) species complex in South Africa provides insight on cryptic speciation. Molecular Phylogenetics and Evolution 82, Part A, 31–42.

McCranie, J.R. & Hedges, S.B. (2013) A new species of Phyllodactylus (Reptilia, Squamata, Gekkonoidea, Phyllodactylidae) from Isla de Guanaja in the Honduran Bay Islands. Zootaxa, 3694 (1), 51–58.
http://dx.doi.org/10.11646/zootaxa.3694.1.3

Minoli, I., Morando, M. & Avila, L.J. (2014) Integrative taxonomy in the Liolaemus fitzingerii complex (Squamata: Liolaemini) based on morphological analyses and niche modeling. Zootaxa, 3856 (4), 501–528.
http://dx.doi.org/10.11646/zootaxa.3856.4.3

Morando, M., Medina, C.D., Avila, L.J., Perez, C.H.F., Buxton, A. & Sites, J.W. Jr. (2014) Molecular phylogeny of the New World gecko genus Homonota (Squamata: Phyllodactylidae). Zoological Scripta, 43 (3), 249–260.
http://dx.doi.org/10.1111/zsc.12052

Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

Nielsen, S.V., Bauer, A.M., Jackman, T.R., Hitchmough, R.A. & Daugherty, C.H. (2011) New Zealand geckos (Diplodactylidae): cryptic diversity in a post-Gondwanan lineage with trans-Tasman affinities. Molecular Phylogenetics and Evolution, 59 (1), 1–22.
http://dx.doi.org/10.1016/j.ympev.2010.12.007

Noble, G.K. (1921) Some new lizards from northwestern Peru. Annals of the New York Academy of Sciences, 29, 133–139.
http://dx.doi.org/10.1111/j.1749-6632.1920.tb55353.x

Noble, G.K. (1924) New lizards from northwestern Peru. Boston Society of Natural History, 5, 107–113.

Oliver, P.M., Adams, M. & Doughty, P. (2010) Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae). BMC Evolutionary Biology, 10 (386), 1–11.
http://dx.doi.org/10.1186/1471-2148-10-386

Padial, J.M. & De la Riva, I. (2009) Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura: Strabomantidae). Zoological Journal of the Linnean Society, 155, 97–122.
http://dx.doi.org/10.1111/j.1096-3642.2008.00424.x

Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16.
http://dx.doi.org/10.1186/1742-9994-7-16

Pepper, M., Doughty, P., Hutchinson, M.N. & Keogh, J.S. (2011) Ancient drainages divide cryptic species in Australia’s arid zone: Morphological and multi-gene evidence for four new species of Beaked Geckos (Rhynchoedura). Molecular Phylogenetics and Evolution, 61 (3), 810–822.
http://dx.doi.org/10.1016/j.ympev.2011.08.012

Peters, W.C.H. (1862) Über einen neuen Phyllodactylus aus Guayaquil. Monatsberichte der königlichen Preussischen Akademie der Wissenschaften zu Berlin, 1862 (November), 626–627.

Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.
http://dx.doi.org/10.1093/bioinformatics/14.9.817

Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877.
http://dx.doi.org/10.1111/j.1365-294x.2011.05239.x

Q&V Ingenieros SAC (2007) Elaboración de resúmenes ejecutivos y fichas de estudio de las centrales hidroeléctricas con potencial para exportación a Brasil. Ministerio de Energía y Minas, Dirección General de Electricidad, 79 pp.

Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6, Available from http://beast.bio.ed.ac.uk/Tracer (accessed 1 Sept. 2016)

Rios, N.E. (2014) Geolocate, a platform for georeferencing legacy collection data. In: 2014 GSA Annual Meeting in Vancouver, British Columbia.

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.
http://dx.doi.org/10.1093/sysbio/sys029

Särkinen, T.E., Marcelo-Peña, J.L., Yomona, A.D., Simon, M.F., Pennington, R.T. & Hughes, C.E. (2011) Underestimated endemic species diversity in the dry inter-Andean valley of the Río Marañón, northern Peru: An example from Mimosa (Leguminosae, Mimosoideae). Taxon, 60 (1), 139–150.

Schliep, K.P. (2011) phangorn: phylogenetic analysis in R. Bioinformatics, 27 (4), 592–593.
http://dx.doi.org/10.1093/bioinformatics/btq706

Siler, C.D., Dececchi , T.A., Merkord, C.L., Davis, D.R. , Christiani, T.J. & Brown, R.M. (2014) Cryptic diversity and population genetic structure in the rare, endemic, forest-obligate, slender geckos of the Philippines. Molecular Phylogenetics and Evolution, 70, 204–209.
http://dx.doi.org/10.1016/j.ympev.2013.09.014

Stattersfield, A.J., Crosby, M.J., Long, A.J. & Wege, D. (1998) Endemic Birds Areas of the World. Priorities for biodiversity conservation. BirdLife International, Cambridge, UK, 860 pp.

Torres-Carvajal, O., Barnes, C.W., Pozo-Andrade, M.J., Tapia, W. & Nicholls, G. (2014) Older than the islands: origin and diversification of Galápagos leaf-toed geckos (Phyllodactylidae: Phyllodactylus) by multiple colonizations.. Journal of Biogeography, 41 (10), 1883–1894.
http://dx.doi.org/10.1111/jbi.12375

Torres-Carvajal, O., Carvajal-Campos, A., Barnes, C.W., Nicholls, G . & Pozo-Andrade, M.J. (2013) A New Andean Species of Leaf-toed Gecko (Phyllodactylidae: Phyllodactylus) from Ecuador. Journal of Herpetology, 47 (2), 384–390.
http://dx.doi.org/10.1670/12-017

Torres-Carvajal, O. & Tapia, W. (2011) First record of the common house gecko Hemidactylus frenatus Schlegel, 1836 and distribution extension of Phyllodactylus reissii Peters, 1862 in the Galápagos. Check List, 7 (4), 470–472.

Uetz, P. & Hošek, J. (2016) The Reptile Database. Available from http://www.reptile-database.org (accessed 4 April 2016)

Venegas, P.J. (2005) Herpetofauna del bosque seco Ecuatorial de Peru: taxonomía, ecología y biogeografía. Zonas Áridas, 9, 9–26.

Venegas, P.J., Townsend, J.H., Koch, C. & Böhme, W. (2008) Two new sympatric species of leaf-toed geckos (Gekkonidae: Phyllodactylus) from the Balsas region of the upper Marañón Valley, Peru. Journal of Herpetology, 42 (2), 386–396.
http://dx.doi.org/10.1670/07-1341.1

Wagner, P., Leaché, A.D. & Fujita, M.K. (2014) Description of four new West African forest geckos of the Hemidactylus fasciatus Gray, 1842 complex, revealed by coalescent species delimitation. Bonn Zoological Bulletin, 63 (1), 1–14.

Werner, F. (1900 [1901]) Reptilien und Batrachier aus Peru und Bolivien. Abhandlungen und Berichte des Königlichen Zoologischen und Anthropologisch-Ethnographischen Museums zu Dresden, 9 (2), 1–14.

Werner, F. (1910 [1909]) Über neue oder seltene Reptilien des Naturhistorischen Museums in Hamburg. II. Eidechsen. Mitteilungen aus dem Naturhistorischen Museum in Hamburg, 15. Jahrgang, 2. Beiheft, 1–46.

Werner, F. (1912) Neue oder seltene Reptilien und Frösche des Naturhistorischen Museums in Hamburg. Mitteilungen aus dem Naturhistorischen Museum in Hamburg, 17. Jahrgang, 2. Beiheft, 1–51.

Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.
http://dx.doi.org/10.1093/bioinformatics/btt499




DOI: http://dx.doi.org/10.11646/zootaxa.4161.1.2

Refbacks

  • There are currently no refbacks.


 
ISSN 1175-5326 (Print Edition) & ISSN 1175-5334 (Online Edition)
Published by Magnolia Press, Auckland, New Zealand