Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-05-13
Page range: 67–100
Abstract views: 243
PDF downloaded: 14

A new cryptic species of fringe-toed lizards from southwestern Arizona with a revised taxonomy of the Uma notata species complex (Squamata: Phrynosomatidae)

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560 Department of Environmental Studies, McDaniel College, 2 College Hill, Westminster, MD 21157
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560 Global Genome Initiative, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St and Constitution Ave NW, Washington DC 20560
Reptilia Dunes Mitochondrial DNA Morphology Phylogeny Sonoran Desert Systematics

Abstract

Fringe-toed lizards (Uma) are among the most specialized lizards in North America, adapted to insular windblown sand habitats in the hyper-arid southwestern deserts, with allopatric distributions, subtle morphological variation, and an unstable taxonomic history. We analyzed a morphological dataset of 40 characters for 65 specimens and a molecular dataset of 2,286 bases from three mitochondrial loci for 92 individuals and interpreted these data alongside published analyses of multi-locus genetic data with the goal of revising the taxonomy of the Uma notata (Baird 1858) species complex. We confirmed that fringe-toed lizards from the Mohawk Dunes in southwestern Arizona (U. sp.) constitute a cryptic species sister to the rest of the complex that can be diagnosed with DNA barcoding and geography, so we describe and name this species Uma thurmanae sp. nov. We also confirmed the evolutionary distinctiveness of U. inornata (Cope 1895), an endangered species endemic to Coachella Valley in southern California. We designate a lectotype for the taxon U. “rufopunctata”, but we put its name in quotation marks to reflect its uncertain taxonomic status with respect to its neighboring species U. cowlesi and U. notata.

 

References

  1. Adest, G. (1977) Genetic relationships in genus Uma (Iguanidae). Copeia, 1977 (1), 47–52.

    https://doi.org/10.2307/1443503

    Alagona, P. & Pincetl, S. (2008) The Coachella Valley multiple species habitat conservation plan: a decade of delays. Environmental Management, 41 (1), 1–11.

    https://doi.org/10.1007/s00267-007-9018-x

    Bagne, K.E., Friggens, M.M. & Finch, D.M. (2011) A system for assessing vulnerability of species (SAVS) to climate change. U.S. Department of Agriculture Forest Service, Fort Collins, 28 pp.

    https://doi.org/10.2737/RMRS-GTR-257

    Bagne, K.E. & Finch, D.M. (2012) Vulnerability of species to climate change in the Southwest: threatened, endangered, and at-risk species at the Barry M. Goldwater Range, Arizona. U.S. Department of Agriculture Forest Service, Fort Collins, 139 pp.

    https://doi.org/10.2737/RMRS-GTR-284

    Baird, S. (1858) Description of new genera and species of North American lizards in the museum of the Smithsonian Institution. Proceedings of the Academy of Natural Sciences of Philadelphia, 1858, 253–256.

    https://doi.org/10.5962/bhl.title.132885

    Beck, W.A. & Hasse, Y.D. (1974) Historical atlas of California. University of Oklahoma Press, Norman, 202 pp.

    Beveridge, C., Kocurek, G., Ewing, R.C., Lancaster, N., Morthekai, P., Singhvi, A.K. & Mahan, S.A. (2006) Development of spatially diverse and complex dune-field patterns: Gran Desierto Dune Field, Sonora, Mexico. Sedimentology, 53 (6), 1391–1409. https://doi.org/10.1111/j.1365-3091.2006.00814.x

    Blount, G. & Lancaster, N. (1990) Development of the Gran Desierto sand sea, northwestern Mexico. Geology, 18 (8), 724–728.

    https://doi.org/10.1130/0091-7613(1990)018%3C0724:dotgds%3E2.3.co;2

    Camp, C. (1916) Notes on the local distribution and habits of the amphibians and reptiles of southeastern California in the vicinity of the Turtle Mountains. University of California Publications in Zoology, 12, 503–544.

    Carpenter, C. (1963) Patterns of behavior in three forms of the fringe-toed lizards (Uma-Iguanidae). Copeia, 1963 (2), 406–412.

    https://doi.org/10.2307/1441361

    Castañeda, M.R. & de Queiroz, K. (2011) Phylogenetic relationships of the Dactyloa clade of Anolis lizards based on nuclear and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 61 (3), 784–800.

    https://doi.org/10.1016/j.ympev.2011.07.004

    Chen, X., Barrows, C. & Li, B. (2006) Is the Coachella Valley fringe-toed lizard (Uma inornata) on the edge of extinction at Thousand Palms Preserve in California? The Southwestern Nationalist, 51 (1), 28–34.

    https://doi.org/10.1894/0038-4909(2006)51[28:itcvfl]2.0.co;2

    Cochran, D.M. (1961) Type specimens of reptiles and amphibians in the U.S. National Museum. Bulletin of the United States National Museum, 220, 1–291.

    https://doi.org/10.5479/si.03629236.220

    Cope, E. (1866) On Reptilia and Batrachia of the Sonoran province of the Nearctic region. Proceedings of the Academy of Natural Sciences of Philadelphia, 18, 300–314.

    Cope, E. (1894) On the iguanian genus Uma. American Naturalist, 28, 434–435.

    https://doi.org/10.1086/276031

    Cope, E. (1895) On the species of Uma and Xantusia. American Naturalist, 29, 938–939.

    Cope, E. (1900) The crocodilians, lizards, and snakes of North America. Annual Report of the United States National Museum 1898, 155–1294.

    Corl, A., Davis, A., Kuchta, S., Comendant, T. & Sinervo, B. (2010) Alternative mating strategies and the evolution of sexual size dimorphism in the Side-Blotched Lizard, Uta stansburiana: A population-level comparative analysis. Evolution, 64 (1), 79–96.

    https://doi.org/10.1111/j.1558-5646.2009.00791.x

    de Queiroz, K. (1989) Morphological and Biochemical Evolution in the Sand Lizards. Ph.D. dissertation. University of California, Berkeley, California, 491 pp.

    de Queiroz, K. (1992) Phylogenetic relationships and rates of allozyme evolution among the lineages of sceloporine sand lizards. Biological Journal of the Linnean Society, 45 (4), 333–362.

    https://doi.org/10.1111/j.1095-8312.1992.tb00648.x

    de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford, pp. 57–75.

    de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886.

    https://doi.org/10.1080/10635150701701083

    de Queiroz, K. (2011) Branches in the lines of descent: Charles Darwin and the evolution of the species concept. Biological Journal of the Linnean Society, 103 (1), 19–35.

    https://doi.org/10.1111/j.1095-8312.2011.01634.x

    de Queiroz, K. & Reeder, T. (2008) Squamata—Lizards. In: Crother, B. (Ed.), Scientific and standard English names of amphibians and reptiles of North America north of Mexico, with comments regarding confidence in our understanding. Society for the Study of Amphibians and Reptiles, Herpetological Circular, 37, pp. 24–45.

    de Queiroz, K. & Reeder, T. (2012) Squamata—Lizards. In: Crother, B. (Ed.), Scientific and standard English names of amphibians and reptiles of North America north of Mexico, with comments regarding confidence in our understanding. Society for the Study of Amphibians and Reptiles, Herpetological Circular, 39, pp. 32–51.

    de Queiroz, K., Reeder, T. & Leaché, A.D. (2017) Squamata (in part)—Lizards. In: Crother, B. (Ed.), Scientific and standard English names of amphibians and reptiles of North America north of Mexico, with comments regarding confidence in our understanding. Society for the Study of Amphibians and Reptiles, Herpetological Circular, 43, pp. 38–58.

    Derkarabetian, S., Castillo, S., Koo, P.K., Ovchinnikovf, S. & Hedin, M. (2019) A demonstration of unsupervised machine learning in species delimitation. Molecular Phylogenetics and Evolution, 139, 106562.

    https://doi.org/10.1016/j.ympev.2019.106562

    Dolby, G.A., Dorsey, R.J. & Graham, M.R. (2019) A legacy of geo-climatic complexity and genetic divergence along the lower Colorado River: Insights from the geological record and 33 desert-adapted animals. Journal of Biogeography, 2019 (46), 2479–2505. https://doi.org/10.1111/jbi.13685

    Edgar, R. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.

    https://doi.org/10.1093/nar/gkh340

    Gottscho, A.D., Marks, S. & Jennings, W.B. (2014) Speciation, population structure, and demographic history of the Mojave Fringe-toed Lizard (Uma scoparia), a species of conservation concern. Ecology and Evolution, 4 (12), 2546–2562.

    https://doi.org/10.1002/ece3.1111

    Gottscho, A.D., Wood, D., Vandergast, A., Lemos-Espinal, J., Gatesy, J. & Reeder, T. (2017) Lineage diversification of fringe-toed lizards (Phrynosomatidae: Uma notata complex) in the Colorado Desert: Delimiting species in the presence of gene flow. Molecular Phylogenetics and Evolution, 106, 103–117.

    https://doi.org/10.1016/j.ympev.2016.09.008

    Hedtke, S., Zamudio, K., Phillips, C., Losos, J. & Brylski, P. (2007) Conservation genetics of the endangered Coachella Valley fringe-toed lizard (Uma inornata). Herpetologica, 63 (4), 411–420.

    https://doi.org/10.1655/0018-0831(2007)63[411:cgotec]2.0.co;2

    Heifetz, W. (1941) A review of the lizards of the genus Uma. Copeia, 1941 (2), 99–111.

    https://doi.org/10.2307/1437440

    Kinsland, G.L. & Lock, B.E. (2001) Proposed lower Colorado River courses prior to 4.3 Ma, Sonora, Mexico. In: Young, R.A. & Spamer, E.E. (Eds.), The Colorado River: Origin and Evolution. Grand Canyon Association Monograph 12. Grand Canyon, Arizona, pp. 107–108.

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452.

    https://doi.org/10.1093/bioinformatics/btp187

    Luke, C. (1986) Convergent evolution of lizard toe fringes. Biological Journal of the Linnean Society, 27 (1), 1–16.

    https://doi.org/10.1111/j.1095-8312.1986.tb01723.x

    Mayhew, W. (1964a) Photoperiodic responses in three species of the lizard genus Uma. Herpetologica, 20 (2), 95–113.

    Mayhew, W. (1964b) Taxonomic status of California populations of the lizard genus Uma. Herpetologica, 20 (3), 170–183.

    Mayhew, W. (1966) Reproduction in the arenicolous lizard Uma notata. Ecology, 47 (1), 9–18.

    https://doi.org/10.2307/1935740

    Mearns, E.A. (1907) Mammals of the Mexican boundary of the United States: a descriptive catalogue of the species of mammals occurring in that region; with a general summary of the natural history, and a list of trees. Part I Families Didelphiidae to Muridae. Bulletin of the United States National Museum, 56, 1–530.

    https://doi.org/10.5479/si.03629236.56.i

    Norris, K. (1958) The evolution and systematics of the iguanid genus Uma and its relation to the evolution of other North American desert reptiles. Bulletin of the American Museum of Natural History, 114, 251–326.

    Pohlert, T. (2014) The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R package. Available from: http://CRAN.R-project.org/package=PMCMR (accessed 11 May 2017)

    Pough, F.H. (1973) Uma inornata. Catalogue of American Amphibians and Reptiles, 126, 1–2.

    Pough, F.H. (1974) Uma scoparia. Catalogue of American Amphibians and Reptiles, 155, 1–2.

    Pough, F.H. (1977) Uma notata. Catalogue of American Amphibians and Reptiles, 197, 1–2.

    Schmidt, K.P. (1922) The amphibians and reptiles of Lower California and the neighboring islands. Bulletin of the American Museum of Natural History, 46, 607707.

    Schmidt, K.P. (1953) A check-list of North American amphibians and reptiles. American Society of Ichthyologists and Herpetologists, Chicago, Illinois, 280 pp.

    Schmidt, K.P. & Bogert, C.M. (1947) A new fringe-footed sand lizard from Coahuila, Mexico. American Museum Novitates, 1339, 19.

    Schneider, C., Rasband, W. & Eliceiri, K. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9 (7), 671675.

    https://doi.org/10.1038/nmeth.2089

    Schulte, J. & de Queiroz, K. (2008) Phylogenetic relationships and heterogeneous evolutionary processes among phrynosomatine sand lizards (Squamata, Iguanidae) revisited. Molecular Phylogenetics and Evolution, 47 (2), 700–716.

    https://doi.org/10.1016/j.ympev.2008.01.010

    Smith, H.M., Langebartel, D.A. & Williams, K.L. (1964) Herpetological type-specimens in the University of Illinois Museum of Natural History. Illinois Biological Monographs, 32, 1–80.

    https://doi.org/10.5962/bhl.title.50204

    Stebbins, R. (1944) Some aspects of the ecology of the iguanid genus Uma. Ecological Monographs, 14 (3), 311–322.

    https://doi.org/10.2307/1948446

    Stebbins, R. (2003) A field Guide to Western Reptiles and Amphibians. Third edition. Houghton Mifflin Company, Boston and New York, 533 pp.

    Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313.

    https://doi.org/10.1093/bioinformatics/btu033

    Trépanier, T. & Murphy, R. (2001) The Coachella Valley fringe-toed lizard (Uma inornata): genetic diversity and phylogenetic relationships of an endangered species. Molecular Phylogenetics and Evolution, 18 (3), 327–334.

    https://doi.org/10.1006/mpev.2000.0881

    U.S. Fish and Wildlife Service [USFWS] (1980) Endangered and threatened wildlife and plants; listing as threatened with critical habitat for the Coachella Valley Fringe-toed Lizard. Federal Register, 45 (188), 63812–63820. Available from: https://www.fws.gov/carlsbad/SpeciesStatusList/CH/19800925_fCH_CVFTL.pdf (accessed 29 May 2017)

    U.S. Fish and Wildlife Service [USFWS] (2010) Coachella Valley Fringe-toed Lizard (Uma inornata): 5-year review: Summary and evaluation. Carlsbad Fish and Wildlife Office, Carlsbad, California, 53 pp. Available from: https://www.fws.gov/carlsbad/SpeciesStatusList/5YR/20100806_5YR_CVFTL.pdf (accessed 29 May 2017)

    Van Denburgh, J. (1922) The reptiles of Western North America, an Account of the Species Known to Inhabit California and Oregon, Washington, Idaho, Utah, Nevada, Arizona, British Columbia, Sonora and Lower California. California Academy of Sciences, San Francisco, 612 pp.

    https://doi.org/10.5962/bhl.title.12504

    Vandergast, A., Wood, D., Thompson, A., Fisher, M., Barrows, C. & Grant, T. (2015) Drifting to oblivion? Rapid genetic differentiation in an endangered lizard following habitat fragmentation and drought. Diversity and Distribution, 22 (3), 344–357.
    https://doi.org/10.1111/ddi.12398

    Venables, W. & Ripley, B. (2002) Modern Applied Statistics with S. 4th Edition. Springer, New York, 446 pp.

    https://doi.org/10.1007/978-0-387-21706-2

    Waters, M.R. (1983) Late Holocene lacustrine chronology and archaeology of ancient Lake Cahuilla, California. Quaternary Research, 19 (3), 373–387.

    https://doi.org/10.1016/0033-5894(83)90042-x

    Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. Available from: http://ggplot2.org (accessed 11 May 2017)

    https://doi.org/10.1007/978-0-387-98141-3

    Wilgenbusch, J. & de Queiroz, K. (2000) Phylogenetic relationships among the phrynosomatid sand lizards inferred from mitochonrial DNA sequences generated by heterogeneous evolutionary processes. Systematic Biology, 49 (3), 592–612.
    https://doi.org/10.1080/10635159950127411

    Winker, C.D. & Kidwell, S.M. (1986) Paleocurrent evidence for lateral displacement of the Pliocene Colorado River delta by the San Andreas fault system, southeastern California. Geology, 14 (9), 788–791.

    https://doi.org/10.1130/0091-7613(1986)14%3C788:PEFLDO%3E2.0.CO;2