The demise of a wonder: Evolutionary history and conservation assessments of the Wonder Gecko Teratoscincus keyserlingii (Gekkota, Sphaerodactylidae) in Arabia

Effective biodiversity conservation planning starts with genetic characterization within and among focal populations, in order to understand the likely impact of threats for ensuring the long-term viability of a species. The Wonder Gecko, Teratoscincus keyserlingii, is one of nine members of the genus. This species is distributed in Iran, Afghanistan, and Pakistan, with a small isolated population in the United Arab Emirates (UAE), where it is classified nationally as Critically Endangered. Within its Arabian range, anthropogenic activity is directly linked to the species’ decline, with highly localised and severely fragmented populations. Here we describe the evolutionary history of Teratoscincus, by reconstructing its phylogenetic relationships and estimating its divergence times and ancestral biogeography. For conservation implications of T. keyserlingii we evaluate the genetic structure of the Arabian population using genomic data. This study supports the monophyly of most species and reveals considerable intraspecific variability in T. microlepis and T. keyserlingii, which necessitate broad systematic revisions. The UAE population of T. keyserlingii likely arrived from southern Iran during the Pleistocene and no internal structure was recovered within, implying a single population status. Regional conservation of T. keyserlingii requires improved land management and natural habitat restoration in the species’ present distribution, and expansion of current protected areas, or establishment of new areas with suitable habitat for the species, mostly in northern Abu Dhabi Emirate.

[1]  J. Pleguezuelos,et al.  An integrative assessment of the diversity, phylogeny, distribution, and conservation of the terrestrial reptiles (Sauropsida, Squamata) of the United Arab Emirates , 2019, PloS one.

[2]  S. Carranza,et al.  Biogeography of Mesalina (Reptilia: Lacertidae), with special emphasis on the Mesalina adramitana group from Arabia and the Socotra Archipelago. , 2019, Molecular phylogenetics and evolution.

[3]  T. Papenfuss,et al.  A molecular phylogenetic hypothesis for the Asian agamid lizard genus Phrynocephalus reveals discrete biogeographic clades implicated by plate tectonics. , 2018, Zootaxa.

[4]  P. Lymberakis,et al.  Cutting the Gordian Knot: Phylogenetic and ecological diversification of the Mesalina brevirostris species complex (Squamata, Lacertidae) , 2017 .

[5]  Peter Uetz,et al.  The global distribution of tetrapods reveals a need for targeted reptile conservation , 2017, Nature Ecology & Evolution.

[6]  M. Akbarpour,et al.  A new species of frog-eyed gecko, genus Teratoscincus Strauch, 1863 (Squamata: Sphaerodactylidae), from southeastern Iran , 2017 .

[7]  Jinliang Wang,et al.  The computer program structure for assigning individuals to populations: easy to use but easier to misuse , 2017, Molecular ecology resources.

[8]  S. Carranza,et al.  Getting off to a good start? Genetic evaluation of the ex situ conservation project of the Critically Endangered Montseny brook newt (Calotriton arnoldi) , 2017, PeerJ.

[9]  D. Rabosky,et al.  Genetic diversity is largely unpredictable but scales with museum occurrences in a species-rich clade of Australian lizards , 2017, Proceedings of the Royal Society B: Biological Sciences.

[10]  A. Bauer,et al.  The measure of success: geographic isolation promotes diversification in Pachydactylus geckos , 2017, BMC Evolutionary Biology.

[11]  Robert Lanfear,et al.  PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. , 2016, Molecular biology and evolution.

[12]  Shai Meiri,et al.  Biases in the current knowledge of threat status in lizards, and bridging the ‘assessment gap’ , 2016 .

[13]  B. Weir,et al.  A Unified Characterization of Population Structure and Relatedness , 2016, Genetics.

[14]  Ben Nichols,et al.  Distributed under Creative Commons Cc-by 4.0 Vsearch: a Versatile Open Source Tool for Metagenomics , 2022 .

[15]  J. Trape,et al.  Out of Africa: Phylogeny and biogeography of the widespread genus Acanthodactylus (Reptilia: Lacertidae). , 2016, Molecular phylogenetics and evolution.

[16]  N. Gemmell,et al.  Genetic Evidence of a Population Bottleneck and Inbreeding in the Endangered New Zealand Sea Lion, Phocarctos hookeri. , 2016, The Journal of heredity.

[17]  Jiajie Zhang,et al.  Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo , 2016, bioRxiv.

[18]  S. Carranza,et al.  Phylogeny and biogeography of Arabian populations of the Persian Horned Viper Pseudocerastes persicus (Duméril, Bibron & Duméril, 1854) , 2016 .

[19]  A. Bauer,et al.  Old but not ancient: coalescent species tree of New Caledonian geckos reveals recent post‐inundation diversification , 2016 .

[20]  S. Carvalho,et al.  Conservation Biogeography of the Sahara‐Sahel: additional protected areas are needed to secure unique biodiversity , 2016 .

[21]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[22]  S. Minton A contribution to the herpetology of West Pakistan. Bulletin of the AMNH ; v. 134, article 2 , 2016 .

[23]  R. Victor The amphibians and reptiles of Oman and the UAE , 2016 .

[24]  M. Jakobsson,et al.  Clumpak: a program for identifying clustering modes and packaging population structure inferences across K , 2015, Molecular ecology resources.

[25]  R. Murphy,et al.  Genetic Assessments and Parentage Analysis of Captive Bolson Tortoises (Gopherus flavomarginatus) Inform Their “Rewilding” in New Mexico , 2014, PloS one.

[26]  J. Červenka,et al.  Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris. , 2014, Zootaxa.

[27]  A. Putnam,et al.  Kinship-based management strategies for captive breeding programs when pedigrees are unknown or uncertain. , 2014, The Journal of heredity.

[28]  Joana Nogueira,et al.  Unravelling biodiversity, evolution and threats to conservation in the Sahara‐Sahel , 2014, Biological reviews of the Cambridge Philosophical Society.

[29]  Ben Collen,et al.  Fiddling in biodiversity hotspots while deserts burn? Collapse of the Sahara's megafauna , 2014 .

[30]  Deren A. R. Eaton,et al.  PyRAD: assembly of de novo RADseq loci for phylogenetic analyses , 2013, bioRxiv.

[31]  G. Ficetola,et al.  Estimating patterns of reptile biodiversity in remote regions , 2013 .

[32]  S. Carranza,et al.  Out of Arabia: A Complex Biogeographic History of Multiple Vicariance and Dispersal Events in the Gecko Genus Hemidactylus (Reptilia: Gekkonidae) , 2013, PloS one.

[33]  A. S. Lobo,et al.  The conservation status of the world's reptiles , 2013 .

[34]  J. C. Brito,et al.  Conquering the Sahara and Arabian deserts: systematics and biogeography of Stenodactylus geckos (Reptilia: Gekkonidae) , 2012, BMC Evolutionary Biology.

[35]  D. Silvestro,et al.  raxmlGUI: a graphical front-end for RAxML , 2012, Organisms Diversity & Evolution.

[36]  V. Trifonov,et al.  Recent mountain building of the central Alpine-Himalayan Belt , 2012, Geotectonics.

[37]  S. Carranza,et al.  A review of the geckos of the genus Hemidactylus (Squamata: Gekkonidae) from Oman based on morphology, mitochondrial and nuclear data, with descriptions of eight new species , 2012 .

[38]  N. Pettorelli,et al.  Forgotten biodiversity in desert ecosystems. , 2012, Science.

[39]  H. Hoekstra,et al.  Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species , 2012, PloS one.

[40]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[41]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[42]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[43]  A. Bauer,et al.  New Zealand geckos (Diplodactylidae): Cryptic diversity in a post-Gondwanan lineage with trans-Tasman affinities. , 2011, Molecular phylogenetics and evolution.

[44]  F. Balloux,et al.  Discriminant analysis of principal components: a new method for the analysis of genetically structured populations , 2010, BMC Genetics.

[45]  Anit Raja Banerjee,et al.  An Introduction to Conservation Genetics , 2010, The Yale Journal of Biology and Medicine.

[46]  B. D. Todd,et al.  The Global Status of Reptiles and Causes of Their Decline , 2010 .

[47]  J. Lamarque,et al.  Global Biodiversity: Indicators of Recent Declines , 2010, Science.

[48]  John Novembre,et al.  Inferring genetic ancestry: opportunities, challenges, and implications. , 2010, American journal of human genetics.

[49]  A. Drummond,et al.  Bayesian Inference of Species Trees from Multilocus Data , 2009, Molecular biology and evolution.

[50]  D. Ojima,et al.  A Review of Climate‐Change Adaptation Strategies for Wildlife Management and Biodiversity Conservation , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[51]  Alexei J. Drummond,et al.  Bayesian Phylogeography Finds Its Roots , 2009, PLoS Comput. Biol..

[52]  E. Shabanian,et al.  Quaternary slip rates along the northeastern boundary of the Arabia–Eurasia collision zone (Kopeh Dagh Mountains, Northeast Iran) , 2009 .

[53]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[54]  R. Frankham Genetic adaptation to captivity in species conservation programs , 2008, Molecular ecology.

[55]  J. Goudet,et al.  A step-by-step tutorial to use HierFstat to analyse populations hierarchically structured at multiple levels. , 2007, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[56]  A. Bauer,et al.  Evidence for Gondwanan vicariance in an ancient clade of gecko lizards , 2007 .

[57]  D. Couvet,et al.  On the expected relationship between inbreeding, fitness, and extinction , 2006, Genetics Selection Evolution.

[58]  H. Stewart Edgell,et al.  Arabian Deserts: Nature, Origin and Evolution , 2006 .

[59]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[60]  J. Boore,et al.  The complete mitochondrial genome of a gecko and the phylogenetic position of the Middle Eastern Teratoscincus keyserlingii. , 2005, Molecular phylogenetics and evolution.

[61]  C. Damgaard,et al.  Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea) , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[63]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[64]  F. Utter,et al.  Marine aquaculture: Genetic potentialities and pitfalls , 2002, Reviews in Fish Biology and Fisheries.

[65]  D. Couvet,et al.  The impact of inbreeding depression on population survival depending on demographic parameters , 2002 .

[66]  M. Searle,et al.  Old origin for an active mountain range: Geology and geochronology of the eastern Hindu Kush, Pakistan , 2001 .

[67]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[68]  J. Searle Phylogeography — The History and Formation of Species , 2000, Heredity.

[69]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[70]  J. Macey,et al.  Vicariant patterns of fragmentation among gekkonid lizards of the genus Teratoscincus produced by the Indian collision: A molecular phylogenetic perspective and an area cladogram for Central Asia. , 1999, Molecular phylogenetics and evolution.

[71]  B. Noon,et al.  Habitat fragmentation , 1999, Oryx.

[72]  T. Herring,et al.  Relatively recent construction of the Tien Shan inferred from GPS measurements of present-day crustal deformation rates , 1996, Nature.

[73]  Kurt Lambeck,et al.  SHORELINE RECONSTRUCTIONS FOR THE PERSIAN GULF SINCE THE LAST GLACIAL MAXIMUM , 1996 .

[74]  Malcolm L. Hunter,et al.  Benchmarks for Managing Ecosystems: Are Human Activities Natural? , 1996 .

[75]  S. Beissinger,et al.  Limitations of Captive Breeding in Endangered Species Recovery , 1996 .

[76]  T. Burkey Extinction Rates in Archipelagoes: Implications for Populations in Fragmented Habitats , 1995 .

[77]  M. Allen,et al.  Paleozoic accretion and Cenozoic redeformation of the Chinese Tien Shan Range, central Asia , 1990 .

[78]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[79]  B. Burchfiel An area of deformation: tectonic evolution of the himalayas and tibet. , 1989, Science.

[80]  M. Nei Molecular Evolutionary Genetics , 1987 .

[81]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[82]  L. Zonenshain,et al.  Present plate tectonics between Turkey and Tibet , 1981 .

[83]  P. Tapponnier,et al.  Mesozoic ophiolites, sutures, and arge-scale tectonic movements in Afghanistan , 1981 .

[84]  Peter Molnar,et al.  Active faulting and cenozoic tectonics of the Tien Shan, Mongolia, and Baykal Regions , 1979 .

[85]  P. Molnar,et al.  Cenozoic Tectonics of Asia: Effects of a Continental Collision: Features of recent continental tectonics in Asia can be interpreted as results of the India-Eurasia collision. , 1975, Science.

[86]  J. Cloudsley-Thompson Biology of Deserts , 1952, Nature.

[87]  N. Ananjeva,et al.  A NEW SPECIES OF FROG-EYED GECKO , GENUS Teratoscincus STRAUCH , 1863 ( SQUAMATA : SAURIA : SPHAERODACTYLIDAE ) , FROM CENTRAL IRAN , 2017 .

[88]  J. Wiens,et al.  Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. , 2016, Molecular phylogenetics and evolution.

[89]  J. Pritchard,et al.  Documentation for structure software : Version 2 . 3 , 2009 .

[90]  E. G. Boulding Genetic Diversity, Adaptive Potential, and Population Viability in Changing Environments , 2008 .

[91]  Reptiles.,et al.  Gecko fauna of the USSR and contiguous regions , 1996 .

[92]  E. Duffey Global biodiversity: Status of the earth's living resources: Compiled by World Conservation Monitoring Centre. Chapman & Hall, London. 1992. 585 pp. ISBN 0-412-47240-6. Price: £29·95. , 1993 .

[93]  M. Searle Geology and tectonics of the Karakoram Mountains , 1991 .

[94]  P. Le Fort Granites in the tectonic evolution of the Himalaya, Karakoram and southern Tibet , 1988, Philosophical transactions of the Royal Society of London. Series A: Mathematical and physical sciences.

[95]  E. N. Arnold The scientific results of the Oman flora and fauna survey 1977 (Dhofar) , 1980 .

[96]  Oman. Ministère de l'information et de la culture The scientific results of the Oman Flora and Fauna Survey 1975 , 1977 .