Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2019-06-18
Page range: 139–154
Abstract views: 199
PDF downloaded: 5

Phylogenetic structure of Holbrookia lacerata (Cope 1880) (Squamata: Phrynosomatidae): one species or two?

Biodiversity Research and Teaching Collection, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843-2258 Natural Resources Institute, Texas A&M University, College Station, TX 77843
Natural Resources Institute, Texas A&M University, College Station, TX 77843
Biodiversity Research and Teaching Collection, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843-2258
Biodiversity Research and Teaching Collection, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843-2258
Department of Ecosystem Science and Management, Texas A&M University, College Station TX 77843-2120
Natural Resources Institute, Texas A&M University, College Station, TX 77843
Natural Resources Institute, Texas A&M University, College Station, TX 77843
Texas Tech University, Department of Natural Resources Management, 2500 Broadway, Lubbock,Texas 79409
The Nature Conservancy, San Antonio, TX 78215,
Bureau of Economic Geology, Jackson School of Geosciences, The University of Texas at Austin, Austin, Texas 78758,USA
Bureau of Economic Geology, Jackson School of Geosciences, The University of Texas at Austin, Austin, Texas 78758,USA
Biodiversity Collections, Department of Integrative Biology, The University of Texas at Austin, Austin, TX 78758-4445 Benjamin J. Labay currently at Siglo Group, Austin, TX 78702
Biodiversity Collections, Department of Integrative Biology, The University of Texas at Austin, Austin, TX 78758-4445
Reptilia Holbrookia lacerata Holbrookia subcaudalis Texas Balcones Escarpment ND2 RAG-1 morphology environmental niche

Abstract

Species delimitation attempts to match species-level taxonomy with actual evolutionary lineages. Such taxonomic conclusions are typically, but not always, based on patterns of congruence across multiple data sources and methods of analyses. Here, we use this pluralistic approach to species delimitation to help resolve uncertainty in species boundaries of phrynosomatid sand lizards of the genus Holbrookia. Specifically, the Spot-tailed Earless Lizard (H. lacerata) was historically divided into a northern (H. l. lacerata) and southern (H. l. subcaudalis) subspecies based on differences in morphology and allopatry, but no research has been conducted evaluating genetic differences between these taxa. In this study, patterns in sequence data derived from two genes, one nuclear and one mitochondrial, for 66 individuals sampled across 18 counties in Texas revealed three strongly supported, reciprocally monophyletic lineages, each comprised of individuals from a single geographic region. Distinct genetic variation evident across two of these regions corresponds with differences in morphology, differences in environmental niche, and lines up with the presumed geographic barrier, the Balcones Escarpment, which is the historical subspecies boundary. The combined evidence from genetics, morphology and environmental niche is sufficient to consider these subspecies as distinct species with the lizards north of the Balcones Escarpment retaining the name Holbrookia lacerata, and those south of the Balcones Escarpment being designated as Holbrookia subcaudalis.

 

References

  1. Archer, S. (1989) Have southern Texas savannas been converted to woodlands in recent history? American Naturalist, 134 (4), 545–561.

    Axtell, R.A. (1956) A solution to the long neglected Holbrookia lacerata problem and the destription of two new subspecies of Holbrookia. Bulletin of the Chicago Academy of Science, 10 (11), 163–179.

    Axtell, R.A. (1968) Holbrookia lacerata. Catalogue of American Amphibians and Reptiles, 56, 1–2.

    Axtell, R.A. (1998) Holbrookia lacerata. Interpretive Atlas of Texas Lizards, 20, 1–11.

    Blaine, R.A. (2008) Biogeography of the North American southwest sand lizards. PhD Dissertation, Washington University, St. Louis, Missouri, 202 pp. [Publication No. 304442278]

    Camper, J.D. & Dixon, J.R. (1994) Geographic variation and systematics of the striped whipsnakes (Masticophis taeniatus complex; Reptilia: Serpentes: Colubridae). Annals of the Carnegie Museum, 63 (1), 1–48.

    Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology, 22 (17), 4369–4383.

    https://doi.org/10.1111/mec.12413

    Cope, E.D. (1880) On the zoological position of Texas. Bulletin of the U. S. National Museum, 17, 1–51.

    https://doi.org/10.5479/si.03629236.17

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772.

    https://doi.org/10.1038/nmeth.2109

    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.

    Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F.T., D’Amen, M., Randin, C., Engler, R., Pottier, J., Pio, D., Dubuis, A. & Pellissier, L. (2017) ecospat: An R package to support spatial analyses and modeling of species niches and distributions. Ecography, 40, 774–787.

    https://doi.org/10.1111/ecog.02671

    Dixon, J.R. (2013) The Amphibians and Reptiles of Texas. 3rd Edition. Texas A&M University, College Station, Texas, 477 pp.

    Elith, J., Graham, C.H., Anderson, R.P., Dudýk, M. & Ferrier, S. (2006) Novel methods improve prediction of species’ distribution models. Ecography, 32, 66–77.

    https://doi.org/10.1111/j.1600-0587.2008.05505.x

    Fick, S.E. & Hijmans, R.J. (2017) Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology. [published online]

    https://doi.org/10.1002/joc.5086

    Fielding, A.H. & Bell, J.F. (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental conservation, 24, 38–49.

    https://doi.org/10.1017/S0376892997000088

    Geyer, C.J. (1991) Markov chain Monte Carlo maximum likelihood. In: Keramidas, E.M. (Ed.), Computing Science and Statistics: Proceedings of the 23rd Symposium on the Interface. Interface Foundation, Fairfax Station, Virginia, pp. 156–163.

    Gould, F.W. (1975) The Grasses of Texas. Texas A&M University Press, College Station, Texas, 654 pp.

    Griffith, G.E., Bryce, S.A., Omernik, J.M., Comstock, J.A., Rogers, A.C., Harrison, B., Hatch, S.L. & Bezanson, D. (2004) Ecoregions of Texas (color poster with map, descriptive text, and photographs). US Geological Survey, Reston, Virginia. [map]

    Guindon, S. & Gascuel O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52 (5), 696–704.

    https://doi.org/10.1080/10635150390235520

    Hammer, Ø. & Harper, D.A.T. (2006) Paleontological Data Analysis. Blackwell, Oxford, 351 pp.

    https://doi.org/10.1002/9780470750711

    Hibbitts, T.D. & Hibbitts, T.J. (2015) Texas Lizards. University of Texas Press, Austin, Texas, 333 pp.

    Hijmans, R.J., Phillips, S., Leathwick, J., Elith, J. & Hijmans, M.R.J. (2017) Package ‘dismo’. Circles, 9, 1.

    Lanfear, R., Calcott, B, Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29 (6), 1695–1701.

    https://doi.org/10.1093/molbev/mss020

    Lanfear, R., Frandsen, P. B.,Wright, A. M., Senfeld, T. & Calcott, B. (2017) Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773.

    https://doi.org/10.1093/molbev/msw260

    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

    Leaché, A.D. & McGuire, J.A. (2006) Phylogenetic relationship of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: Evidence for a misleading mitochondrial gene tree. Molecular Phylogenetics and Evolution, 39 (3), 628–644.

    https://doi.org/10.1016/j.ympev.2005.12.016

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Knowles, L.L. & Carstens, B.C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology, 56 (6), 887–895.

    https://doi.org/10.1080/10635150701701091

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.

    https://doi.org/10.1093/molbev/msw054

    Macey, J.R., Larson, A., Ananjeva, N.B. & Papenfuss, T.J. (1997) Evolutionary shifts in three major structural features of the mitochondrial genome among iguanian lizards. Journal of Molecular Evolution, 44 (6), 660–674.

    https://doi.org/10.1007/PL00006190

    Nix, H.A. (1986) A biogeographic analysis of Australian elapid snakes. Atlas of elapid snakes of Australia, 7, 4–15.

    Phillips, S.J., Dudík, M. & Schapire, R.E. (2017) Maxent software for modeling species niches and distributions. Version 3.4.1. Available from: http://biodiversityinformatics.amnh.org/open_source/maxent/ (accessed 10 November 2017)

    Rambaut A. & Drummond A.J. (2007) Tracer. Version 1.4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 6 May 2019)

    Roelke, C.E., Maldonado, J.A., Pope, B.W., Firneno Jr., T.J., LaDuc, T.J., Hibbitts, T.J., Ryberg, W.A., Rains, N.D. & Fujita, M.K. (2018) Mitochondrial genetic variation within and between Holbrookia lacerata lacerata and Holbrookia lacerata subcaudalis, the Spot-tailed Earless Lizard of Texas. Journal of Natural History, 52, 1017–1027.

    https://doi.org/10.1080/00222933.2018.1436726

    Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.

    https://doi.org/10.1093/bioinformatics/btg180

    Schlick-Steiner, B.C., Steiner, F.M., Seifert, B., Stauffer, C., Christian, E. & Crozier, R.H. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.

    https://doi.org/10.1146/annurev-ento-112408-085432

    Schoener, T.W. (1968) Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49, 704–726.

    https://doi.org/10.2307/1935534

    Schulte, J.A. & 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

    Scott, N.J. (1996) Evolution and management of the North American grassland herpetofauna. In: Finch, D.M. (Ed.), Ecosystem disturbance and wildlife conservation in western grasslands—A symposium proceedings, Albuquerque, New Mexico, 22–26 September, 1994. General Technical Report RM-GTR-285. USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, Colorado, pp. 40–53.

    Smith, H.R. & Buechner, H.K. (1947) The influence of the Balcones Escarpment on the distribution of amphibians and reptiles in Texas. Bulletin of the Chicago Academy of Science, 8, 1–16.

    Stejneger, L. (1890) Part V.—Annotated list of reptiles and batrachians collected by Dr. C. Hart Merriam and Vernon Bailey on the San Francisco Mountain Plateau and desert of the Little Colorado, Arizona, with descriptions of new species. North American Fauna, 103–118.

    https://doi.org/10.3996/nafa.3.0006

    Stephens M., Smith N. & Donnelly P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68 (4), 978–989.

    https://doi.org/10.1086/319501

    Tix, D. (2000) Cenchrus ciliaris invasion and control in southwestern US grasslands and shrublands. Restoration and Reclamation Review, 6 (1), 1–6.

    USFWS (2011) Endangered and threatened wildlife and plants; 90-day finding on a petition to list the Spot-tailed Earless Lizard as endangered or threatened. Federal Register, 76 (100), 30082–30087.

    Van der Vaart, A.W. (1998) Asymptotic statistics. Cambridge Univ. Press, Cambridge.

    https://doi.org/10.1017/CBO9780511802256

    VanDerWal, J., Falconi, L., Januchowski, S., Shoo, L. & Storlie, C. (2014) SDMTools: Species Distribution Modelling Tools: Tools for processing data associated with species distribution modelling exercises. R package version, 1 pp. Available from: https://www.rforge.net/SDMTools/ (accessed 6 May 2019)

    Varela, S., Anderson, R.P., García-Valdés, R. & Fernández-González, F. (2014) Environmental filters reduce the effects of sampling bias and improve predictions of ecological niche models. Ecography, 37, 1084–1091.

    https://doi.org/10.1111/j.1600-0587.2013.00441.x

    Warren, D.L., Glor, R.E. & Turelli, M. (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62, 2868–2883.

    https://doi.org/10.1111/j.1558-5646.2008.00482.x

    Wiens, J.J. & Penkrot, T.A. (2002) Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology, 51 (1), 69–91.

    https://doi.org/10.1080/106351502753475880

    Wiens, J.J., Kuczynski, C.A., Arif, S. & Reeder, T.W. (2010) Phylogenetic relationships of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus. Molecular Phylogenetics and Evolution, 54 (1), 150–161.

    https://doi.org/10.1016/j.ympev.2009.09.008

    Wilgenbusch, J. & De Queiroz, K. (2000) Phylogenetic relationships among the phrynosomatid sand lizards inferred from mitochondrial DNA sequences generated by heterogeneous evolutionary processes. Systematic Biology, 49 (3), 592–612.

    https://doi.org/10.1080/10635159950127411