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Cytonuclear Discordance, Cryptic Diversity, Complex Histories, and Conservation Needs in Vietnamese Bent-toed Geckos of the Cyrtodactylus irregularis Species Complex

Sang Ngoc Nguyen, Wei-Wei Zhou, Thanh-Ngan Thi Le, Anh-Dao Thi Tran, Jie-Qiong Jin, Ba Dinh Vo, Luan Thanh Nguyen, Tao Thien Nguyen, Truong Quang Nguyen, Dat Duc Hoang, Nikolai L. Orlov, Jing Che, Robert Murphy, Ya-Ping Zhang

Abstract


Examples of cytonuclear discordance (CD), i.e. differing branching patterns from mitochondrial and nuclear DNA data, are increasing. This raises concerns about combining data from the two genomes for the purpose of reconstructing phyletic history. Because of this, we explore the efficacy of DNA barcoding based on the gene cytochrome c oxidase subunit I (COI; Entrez COX1) from the perspective of two nuclear DNA (nDNA) loci: RPL35 and RAG1. Our analyses use 164 samples of Vietnamese bent-toed geckos of the Cyrtodactylus irregularis species complex (Reptilia: Gekkonidae) collected from 24 localities and 306 new sequences. DNA barcoding infers the presence of ten described species and identifies at least 11 unknown lineages from different areas. K2P genetic distances between sites average 16.6 ± 4.6%. Phylogenetic analyses of nuclear DNA data resolve two strongly supported main clades that correspond with northern and southern groups of geckos and presence or absence of enlarged fermoral scale rows. The matrilineal genealogy and nDNA phylogeny are concordant in resolving major lineages, yet trees derived from the two sets of data, and a combined mtDNA-nDNA dataset, are significantly incompatible (AU test: p < 0.01). The extent of CD precludes combining the two genomes for a single analysis. Analyses of both genomes suggest the presence of at least five undescribed cryptic species. Geckos at one site, Ta Kou Mountain, have a complex history involving the unification of two divergent matrilines (K2P = 10.2%). Analyses of nDNA markers alone does not recover this event because gene flow has erased the historical signal. Finally, the independent and geographically isolated lineages face a battle for survival owing to continued habitat destruction. Urgent conservation planning and implementation is necessary for many sites.

Keywords


COI; DNA barcoding; matrilineal genealogy; phylogeny; Vietnam

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References


Ardura A., Linde A. R., Moreira J. C., and Garicia-Vazquez E. (2010), «DNA barcoding for conservation and management of Amazonian commercial fish», Biol. Conserv., 143, 1438 – 1443.

Bain R. H. and Hurley M. M. (2011), «A biogeographic synthesis of the amphibians and reptiles of Indochina», Bull. Am. Mus. Nat. Hist., 360, 1 – 138.

Cai J. X. and Zhang K. J. (2009), «A new model for the Indochina and South China collision during the late Permian to the middle Triassic», Tectonophysics, 467, 35 – 43.

Carbayo F. and Marques A. C. (2011), «The costs of describing the entire animal kingdom», Trends Ecol. Evol., 26, 154 – 155.

Che J., Chen H. M., Yang J. X., Jin J. Q., Jiang K., Yuan Z. Y., Murphy R. W., and Zhang Y. P. (2012), «Universal COI primers for DNA barcoding amphibians», Mol. Ecol. Resour., 12, 247 – 258.

Clare E. L., Lim B. K., Fenton M. B., and Hebert P. D. N. (2011), «Neotropical bats: estimating species diversity with DNA barcodes», PLoS ONE, 6, e22648.

David P., Teynié A., and Ohler A. (2004), «A new species of Cyrtodactylus Gray 1827 (Reptilia: Squamata: Gekkonidae) from southern Laos», Raffles Bull. Zool., 52, 621 – 627.

Davy C. M., Mendez de la Cruz F. R., Lathrop A., and Murphy R. W. (2011), «Seri Indian traditional knowledge and molecular biology agree: no express train for island-hopping spiny-tailed iguanas in the Sea of Cortés», J. Biogeogr., 38, 272 – 284.

Derycke S., Vanaverbeke J., Rigaux A., Backeljau T., and Moens T. (2010), «Exploring the use of Cytochrome oxidase c subunit 1 (COI) for DNA barcoding of free-living marine nematodes», PLoS ONE, 5, e13716.

Ding L., Gan X. N., He S. P., and Zhao E. M. (2011), «A phylogeographic, demographic and historical analysis of the short-tailed pit viper (Gloydius brevicaudus): evidence for early divergence and late expansion during the Pleistocene», Mol. Ecol., 20, 1905 – 1922.

Drummond A. J. and Rambaut A. (2007), «BEAST: Bayesian evolutionary analysis by sampling trees», BMC Evol. Biol., 7, 214.

Excoffier L. and Lischer H. E. L. (2010), «Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows», Mol. Ecol. Resour., 10, 564 – 567.

Felsenstein J. (1989), «PHYLIP – Phylogeny inference package (version 3.k2)», Cladistics, 5, 164 – 166.

Felsenstein J. (2004), Inferring phylogenies, Sinauer Associates, Sunderland, MA.

Fisher-Reid M. C. and Wiens J. J. (2011), «What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodon salamanders and 13 other vertebrate clades», BMC Evol. Biol., 11, 300.

Flot J. F. (2010), «SEQPHASE: a web tool for interconverting phase input/output files and fasta sequence alignments», Mol. Ecol. Resour., 10, 162 – 166.

Francis C. M., Borisenko A. V., Ivanova N. V., Eger J. L., Lim B. K., Guillen-Servent A., Kruskop S. V., Mackie I., and Hebert P. D. N. (2010), «The role of DNA barcodes in understanding and conservation of mammal diversity in Southeast Asia», PLoS ONE, 5, e12575.

Gamble T., Bauer A. M., Collo G. R., Greenbaum E., Jackman T. R., Vitt L. J., and Simons A. M. (2011), «Coming to America: multiple origins of New World geckos», J. Evol. Biol., 24, 231 – 244.

Gao Y., Wang S. Y., Luo J., Murphy R. W., Du R., Wu S. F., Zhu C. L., Li Y., Poyarkov A. D., Nguyen S. N., Luan P. T., and Zhang Y. P. (2012), «Quaternary palaeoenvironmental oscillations drove the evolution of East Asian Carassius auratus complex (Carassius, Cypriniformes, Cyprinidae)», J. Biogeogr., 39, 2264 – 2278.

Geissler P., Nazarov R., Orlov N. L., Böhme W., Phung M. T., Nguyen Q. T., and Ziegler T. (2009), «A new species of the Cyrtodactylus irregularis complex (Squamata: Gekkonidae) from southern Vietnam», Zootaxa, 2161, 20 – 32.

Gernhard T. (2008), «The conditioned reconstructed process», J. Theor. Biol., 253, 769 – 778.

Goloboff P. A., Farris J. S., and Nixon K. C. (2008), «TNT, a free program for phylogenetic analysis», Cladistics, 24, 774 – 786.

Gonzalez M. A., Baraloto C., Engel J., Mori S. A., Pétronelli P., Riéra B., Roger A., Thébaud C., and Chave J. (2009), «Identification of Amazonian Trees with DNA Barcodes», PLoS ONE, 4, e7483.

Green R. E., Krause J., Briggs A. W., Maricic T., Stenzel U., Kircher M., Patterson N., Li H., Zhai W., Fritz M. H., and Hansen N. F. (2010), «A draft sequence of the Neandertal genome», Science, 328, 710 – 722.

Hall B. G. (2008), Phylogenetic trees made easy: a how-to manual, Sinauer Associates, Sunderland, MA.

Hanke M. and Wink M. (1994), «Direct DNA sequencing of PCR-amplified vector inserts following enzymatic degradation of primer and dNTPs», Biotechniques, 17, 858 – 860.

Hebert P. D. N., Cywinska A., Ball S. L., and deWaard J. R. (2003a), «Biological identifications through DNA barcodes», Proc. R. Soc. Lond. B, 270, 313 – 321.

Hebert P. D. N., Ratnasingham S., and deWaard J. R. (2003b), «Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species», Proc. R. Soc. Lond. B, Suppl. 1, S96 – S99.

Hebert P. D. N., Stoeckle M. Y., Zemlak T. S., and Francis C. M. (2004), «Identification of birds through DNA barcodes», PLoS Biol., 2, e312.

Hebert P. D. N., deWaard J. R., and Landry J. F. (2009), «DNA barcodes for 1/1000 of the animal kingdom», Biol. Lett., 6, 359 – 362.

Heidrich A., Rösler H., Vu N. T., Böhme W., and Ziegler T. (2007), «Another new Cyrtodactylus (Squamata: Gekkonidae) from Phong Nha-Ke Bang National Park, central Truong Son, Vietnam», Zootaxa, 1445, 35 – 48.

Hewitt G. M. (2000), «The genetic legacy of the Quaternary ice ages», Nature, 405, 907 – 913.

Hewitt G. M. (2004) «Genetic consequences of climatic oscillations in the Quaternary», Philos. Trans. Roy. Soc. Lond. Ser. B. Biol. Sci., 359, 183 – 195.

Hillis D. M. and Bull J. J. (1993), «An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis», Syst. Biol., 42, 182 – 192.

Hubert N., Hanner R., Holm E., Mandrak N. E., Taylor E., Burridge M., Watkinson D., Dumont P., Curry A., Bentzen P., and Zhang J. (2008), «Identifying Canadian freshwater fishes through DNA barcodes», PLoS ONE, 3, e2490.

Kimura M. (1980), «A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences», J. Mol. Evol., 16, 111 – 120.

Liu K. (1988), «Quaternary history of the temperate forests of China», Quatern. Sci. Rev., 7, 1 – 20.

Mabragana E., Astarloa J. M. D. A., Hanner R., Zhang J., and Castro M. G. (2011), «DNA barcoding identifies argentine fishes from marine and brackish waters», PLoS ONE, 6, e28655.

Metcalfe I. (1998), «Palaeozoic and Mesozoic geological evolution of the SE Asian region: multidisciplinary constraints and implications for biogeography», in: R. Hall and J. D. Holloway (eds.), Biogeography and Geological Evolution of SE Asia, Backhuys Publishers, Leiden, the Netherlands, pp. 25 – 41.

Murphy R. W., McCollum F. C., Gorman G. C., and Thomas R. (1984), «Genetics of hybridizing populations of Puerto Rican Sphaerodactylus», J. Herpetol., 18, 93 – 105.

Murphy R. W. and Aguirre-Léon G. (2002), «The non-avian reptiles: origins and evolution», in: T. J. Case, M. L. Cody and E. Ezcurra (eds.), A New Island Biogeography of the Sea of Cortés, Oxford Univ. Press, pp. 181 – 228.

Murphy R. W., Crawford A. J., Bauer A. M., Che J., Donnellan S. C., Fritz U., Haddad C. F., Nagy Z. T., Poyarkov N. A., Vences M., and Wang W. Z. (2013), «Cold Code: the global initiative to DNA barcode amphibians and nonavian reptiles», Mol. Ecol. Resour., 13, 161 – 167.

Murphy R. W. and Méndez de la Cruz F. R. (2010), «The herpetofauna of Baja California and its associated islands: a conservation assessment and priorities», in: L. D. Wilson, L. H. Townsend and J. D. Johnson (eds.), Conservation of Mesoamerican amphibians and reptiles, Eagle Mountain Publishing, LC, Eagle Mountain, Utah, pp. 238 – 273.

Nagy Z. T., Sonet G., Glaw F., and 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.

Nazarov A. R., Orlov N. L., Nguyen N. S., and Ho T. C. (2008), «Taxonomy of naked-toes geckos Cyrtodactylus irregularis complex of South Vietnam and description of a new species from Chu Yang Sin Natural Park (Krong Bong district, Dac Lac Province, Vietnam)», Russ. J. Herpetol., 15, 141 – 156.

Nazarov R, Poyarkov N. A., Orlov N. L., Phung T. M., Nguyen T. T., Hoang D. M., and Ziegler T. (2012), «Two new cryptic species of the Cyrtodactylus irregularis complex (Squamata: Gekkonidae) from southern Vietnam», Zootaxa, 3302, 1 – 24.

Ngo T. V. (2013), «Cyrtodactylus dati, a new forest dwelling bent-toed gecko (Squamata: Gekkonidae) from southern Vietnam», Zootaxa, 3616, 151 – 164.

Ngo T. V. and Bauer A. M. (2008), «Descriptions of two new species of Cyrtodactylus Gray 1827 (Squamata: Gekkonidae) endemic to southern Vietnam», Zootaxa, 1715, 27 – 42.

Nguyen S. N., Le T. N. T., Tran T. A. D., Orlov N. L., Lathrop A., MacCulloch R. D., Le T. D. T., Jin J. Q., Nguyen L. T., Nguyen T. T., Hoang D. D., Che J., Murphy R. W., and Zhang Y. P. (2013), «Phylogeny of the Cyrtodactylus irregularis species complex (Squamata: Gekkonidae) from Vietnam with the description of two new species», Zootaxa, 3737, 399 – 414.

Nguyen S. N., Yang J. X., Le T. N. T., Nguyen L. T., Orlov N. L., Hoang C. V., Nguyen T. Q., Jin J. Q., Rao D. Q., Hoang T. N., Che J., Murphy R. W., and Zhang Y. P. (2014), «DNA barcoding of Vietnamese bent-toed geckos (Squamata: Gekkonidae: Cyrtodactylus) and the description of a new species», Zootaxa, 3784, 48 – 66.

Nylander J. A. A. (2004), MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala University.

Ohno S., Stenius C., Christian L., and Schipmann G. (1969), «De novo mutation-like events observed at the 6GPD locus in Japanese quail, and the principle of polymorphism breeding more polymorphism», Biochem. Genet., 3, 417 – 428.

Park D. S., Foottit R., Maw E., and Hebert P. D. N. (2011), «Barcoding bugs: DNA-based identification of the true bugs (Insecta: Hemiptera: Heteroptera)», PLoS ONE, 6, e18749.

Rambaut A. and Drummond A. J. (2007), Tracer v1.k4. Available from http://beast.kbio.ked.kac.kuk/Tracer

Ronquist R. R. and Huelsenbeck J. P. (2003), «MrBayes 3: Bayesian phylogenetic inference under mixed models», Bioinformatics, 19, 1572 – 1574.

Rösler H., Vu N. T., Nguyen Q. T., Ngo V. T., and Ziegler T. (2008), «A new Cyrtodactylus (Squamata: Gekkonidae) from central Vietnam», Hamadryad, 33, 48 – 63.

Sambrook J., Fritsch E. F., and Maniatis T. (1989), Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

Schneider N., Phung T. M., Le M. D., Nguyen T. Q., and Ziegler T. (2014), «A new Cyrtodactylus (Squamata: Gekkonidae) from Khanh Hoa Province, southern Vietnam», Zootaxa, 3785, 518 – 532.

Shi Y. F., Ren B., Wang J., and Derbyshire E. (1986), «Quaternary glaciation in China», Quatern. Sci. Rev., 5, 503 – 507.

Shimodaira H. (2002), «An approximately unbiased test of phylogenetic tree selection», Syst. Biol., 51, 492 – 508.

Shimodaira H. and Hasegawa M. (2001), «CONSEL: for assessing the confidence of phylogenetic tree selection», Bioinformatics, 17, 1246 – 1247.

Shokralla S., Zhou X., Janzen D. H., Hallwachs W., Landry J. F., Jacobus L. M., and Hajibabaei M. (2011), «Pyrosequencing for mini-barcoding of fresh and old museum specimens», PLoS ONE, 6, e21252.

Siler C. D., Oask J. R., Esselstyn J. A., Diesmos A. C., and Brown R. M. (2010), «Phylogeny and biogeography of Philippine bent-toed geckos (Gekkonidae: Cyrtodactylus) contradict an prevailing model of Pleistocene diversification», Mol. Phylogen. Evol., 55, 699 – 710.

Siler C. D., Oaks J. R., Welton L. J., Linkem C. W., Swab J. C., Diesmos A. C., and Brown R. M. (2012), «Did geckos ride the Palawan raft to the Philippines?» J. Biogeogr., 39, 1217 – 1234.

Smith M. A. (1921), «New or little-known reptiles and batrachians from southern Annam (Indo-China)», Proc. Zool. Soc. Lond., 11, 423 – 440.

Smith M. A. (1935), The fauna of British India, including Ceylon and Burma. Reptilia and Amphibia. Vol. II. Sauria, Taylor and Francis, London.

Song H., Buhay J. E., Whiting M. F., and Crandall K. A. (2008), «Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified», Proc. Natl. Acad. Sci. USA, 105, 13486 – 13491.

Stamatakis A. S., Hoover P., and Rougemont J. (2008), «A rapid bootstrap algorithm for the RAxML web servers», Syst. Biol., 57, 758 – 771.

Stephens M., Smith N. J., and Donnelly P. (2001), «A new statistical method for haplotype reconstruction from population data», Am. J. Hum. Gen., 68, 978 – 989.

Swofford D. L. (2002), PAUP*. Phylogenetic analysis using parsimony (* and other methods), Sinauer Associates, Sunderland, MA.

Tamura K., Dudley J., Nei M., and Kumar S. (2007), «MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0», Mol. Biol. Evol., 24, 1596 – 1599.

Thompson J. D., Higgins D. G., and Gibson T. J. (1994), «CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice», Nucl. Acids Res., 22, 4673 – 4680.

Towes D. P. L. and Brelsford A. (2012), «The biogeography of mitochondrial and nuclear discordance in animals», Mol. Ecol., 21, 3907 – 3930.

Upton D. E. and Murphy R. W. (1997), «Phylogeny of the side-blotched lizards (Phrynosomatidae: Uta) based on mtDNA sequences: support for a midpeninsular seaway in Baja California», Mol. Phylogen. Evol., 8, 104 – 113.

Usuki T., Lan C. Y., Yui T. F., Iizuka Y., Vu V. T., Tran T. A., Okamoto K., Wooden J. L., and Liou J. G. (2009), «Early Paleozoic medium-pressure metamorphism in central Vietnam: evidence from SHRIMP U-Pb zircon ages», Geosci. J., 13, 245 – 256.

Uetz P., Freed P., and Hosek J. (eds.) (2017), The Reptile Database, URL: http://www.reptile-database.org (accessed on 3 April, 2017).

Witt J. D. S., Threloff D. L., and Hebert P. D. N. (2006), «DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation», Mol. Ecol., 15, 3073 – 3082.

Xia Y. U. N., Gu H. F., Peng R. U. I., Chen Q. I. N., Zheng Y. C., Murphy R. W., and Zeng X. M. (2012), «COI is better than 16S rRNA for DNA barcoding Asiatic salamanders (Amphibia: Caudata: Hynobiidae)», Mol. Ecol. Resour., 12, 48 – 56.

Yan F., Jiang K., Chen H., Fang P., Jin J., Li Y., Wang S., Murphy R. W., Che J., and Zhang Y. (2011), «The matrilineal history of the Rana longicrus species group (Rana, Ranidae, Anura) and the description of a new species from Hunan province, southern China», Asian Herpetol. Res., 2, 61 – 71.

Yule G. U. (1925), «A mathematical theory of evolution, based on the conclusions of Dr. J. C. Willis, F. R. S»., Philos. Trans. R. Soc. Lond. Ser. B. Biol. Sci., 213, 21 – 87.

Zhang D. R., Chen M. Y., Murphy R. W., Che J., Pang J. F., Hu J. F., Lou L., Wu S. J., Ye H., and Zhang Y. P. (2010), «Genealogy and palaeodrainage basins in Yunnan province: phylogeography of the Yunnan spiny frog, Nanorana yunnanensis (Dicroglossidae)», Mol. Ecol., 19, 3406 – 3420.




DOI: https://doi.org/10.30906/1026-2296-2017-24-2-133-154

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