Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2018-06-21
Page range: 283–298
Abstract views: 107
PDF downloaded: 60

Molecular evidence for conspecificity of two desert Liolaemus lizards (Iguania: Liolaemidae)

Centro de Investigación en Medio Ambiente (CENIMA), Universidad Arturo Prat, Casilla 121, Iquique, Chile Laboratorio de Herpetología, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción Programa de Doctorado en Sistemática y Biodiversidad, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción
Laboratorio de Herpetología, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción
Laboratorio de Investigación y Gestión Ambiental, LABIGAM Universidad de Antofagasta, Antofagasta, Avda. Universidad de Antofagasta 02800
Red de Observadores de Aves y Vida Silvestre de Chile
Laboratorio de Herpetología, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción
Reptilia Atacama Desert synonymy species delimitation Liolaemus audituvelatus L. manueli Phrynosaura

Abstract

Liolaemus audituvelatus (Núñez & Yáñez 1983) and L. manueli (Núñez, Navarro, Garín, Pincheira-Donoso & Meriggio 2003) are endemic species of the Atacama Desert of northern Chile that belong to the montanus group. Both species are considered cryptic from each other and can only be distinguished by their distribution ranges and karyotypes. Originally, there was a wide separation zone between their known distribution ranges, but later collections reduced the gap from 430 km to only 150 km. In this study, we review the geographic information about both species and report new localities within the distribution gap, where species identification becomes difficult. We performed a molecular phylogenetic analysis and applied several species delimitation methods to reassess the taxonomic status of both nominal species and new intermediate populations. Our analyses support the placement of L. manueli in the synonymy of L. audituvelatus. We discuss the biogeographic and conservation implications of this new synonymy.

 

References

  1. Abdala, C. & Quinteros, A. (2014) Los últimos 30 años de estudios de la familia de lagartijas más diversa de Argentina. Actualización taxonómica y sistemática de Liolaemidae. Cuadernos de Herpetología, 28 (2), 55–82.

    Aguilar, C., Wood, P.L., Belk, M.C., Duff, M.H. & Sites, J.W. (2016) Different roads lead to Rome: Integrative taxonomic approaches lead to the discovery of two new lizard lineages in the Liolaemus montanus group (Squamata: Liolaemidae). Biological Journal of the Linnean Society, 120 (2), 448–467.
    https://doi.org/10.1111/bij.12890

    Aiassa, D. & Gorla, N. (2010) Cariotipos de Liolaemus quilmes y Liolaemus wiegmannii y comparación con otros taxones del grupo boulengeri. Multequina, 19, 43–52.

    Aiassa, D., Gorla, N., Ávila, L. & Martori, R. (1999) Cariotipo de Liolaemus darwini (Squamata: Tropiduridae). FACENA, 15, 137–144.

    Aiassa, D., Martori, R. & Gorla, N. (2005) Citogenética de los lagartos del género Liolaemus (Iguania: Liolaemidae) de América del Sur. Cuadernos de Herpetología, 18 (2), 23–36.

    Aparicio, J. & Ocampo, M. (2010) Liolaemus grupo montanus Etheridge, 1995 (Iguania - Liolaemidae). Novedad zoogeográfica. Cuadernos de Herpetología, 24 (2), 133–135.

    Cei, J.M. (1993) Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, Puna y Pampas. Museo Regionale di Scienze Naturali di Torino, Monografie 14, 1–949.

    Cei, J.M., Etheridge, R.E. & Videla, F. (1985) Especies nuevas de iguanidos del noroeste de la provincia de San Juan (Reserva Provincial San Guillermo), Argentina. Deserta, 7, 316–323.

    Donoso-Barros, R. (1966) Reptiles de Chile. Ediciones Universidad de Chile, Santiago. cxliv + 458 pp.

    Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
    https://doi.org/10.1186/1471-2105-5-113

    Etheridge, R. (1995) Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae). American Museum Novitates, 3142, 1–34.

    Frost, D.R. & Etheridge, R. (1989) A phylogenetic analysis and taxonomy of iguanian lizards (Reptilia: Squamata). University of Kansas Museum Natural History, Miscellaneous Publications 81, 1–65.

    GBIF.org (28 December 2016) GBIF Occurrence Download. Available from: https://www.gbif.org/occurrence/download/0045186-160910150852091 (accessed 11 May 2018)

    Green, P.J. (1995) Reversible jump Markov chain Monte Carlo computation and Bayesian model determination. Biometrika, 82, 711–732.
    https://doi.org/10.1093/biomet/82.4.711

    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Iturra, P., Veloso, V., Espejo, P. & Navarro, P. (1994) Karyotypic and meiotic evidence for a Robertsonian chromosome polymorphism in the lizard Liolaemus fuscus (Tropiduridae, Sauria). Revista Brasileira de Genetica, 17 (2), 171–174.

    Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A. & Flouri, T. (2017) Multi-rate Poisson Tree Processes for single-locus species delimitation under Maximum Likelihood and Markov Chain Monte Carlo. Bioinformatics, 33 (11), 1630–1638.

    https://doi.org/10.1093/bioinformatics/btx025

    Kocher, T.D., Thomas, W.K., Meyer, A., Eduards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. PNAS, Proceedings of the National Academy of Sciences, 86, 6196–6200.
    https://doi.org/10.1073/pnas.86.16.6196

    Lamborot, M. & Alvarez-Sarret, E. (1989) Karyotypic characterization of some Liolaemus lizards in Chile (Iguanidae). Genome, 32, 393–403.
    https://doi.org/10.1139/g89-461

    Lamborot, M. & Alvarez-Sarret, E. (1993) Karyotypic variation within and between populations of Liolaemus monticola (Tropiduridae) separated by the Maipo River in the Coastal Range of Central Chile. Herpetologica, 49, 435–449.

    Lamborot, M. & Vásquez, M. (1998) A Triploid Lizard (Liolaemus gravenhorsti) from Chile. Journal of Herpetology, 32 (4), 617–620.
    https://doi.org/10.2307/1565225

    Lamborot, M. (1991) Karyotypic variation among populations of Liolaemus monticola (Tropiduridae), separated by riverine barriers at the Andean Range. Copeia, 1991, 1044–1059.
    https://doi.org/10.2307/1446100

    Lamborot, M. (1993) Chromosomal evolution and speciation in some Chilean lizards. Evolución Biológica, 7, 133–151.

    Lamborot, M. (1998) A new derived and highly polymorphic chromosomal race of Liolaemus monticola (Iguanidae) from the “Norte Chico” of Chile. Chromosome Research, 6, 247–254.
    https://doi.org/10.1023/A:1009267821416

    Lamborot, M. (2001) Karyotypic polymorphism and evolution within and between the Liolaemus monticola (Iguanidae) “northern 2n=38-40” chromosome race populations in central Chile. Revista Chilena de Historia Natural, 74, 121–138.
    https://doi.org/10.4067/S0716-078X2001000000017

    Lamborot, M., Alvarez, E., Campos, I. & Espinoza, A. (1981) Karyotypic characterization of three chilean subspecies of Liolaemus monticola. Journal Heredity, 72, 328–334.
    https://doi.org/10.1093/oxfordjournals.jhered.a109516

    Lamborot, M., Espinoza, A. & Alvarez, E. (1979) Karyotypic variation in Chilean lizards of the genus Liolaemus (Iguanidae). Experientia, 35, 593–594.

    Lamborot, M., Manzur, M.E. & Alvarez-Sarret, E. (2006) Triploidy and mosaicism in Liolaemus chiliensis (Sauria: Tropiduridae). Genome, 49 (5), 445–53.
    https://doi.org/10.1139/g05-122

    Laurent, R. (1983) Contribución al conocimiento de la estructura taxonómica del género Liolaemus Wiegmann (Iguanidae). Boletín de la Asociación Herpetológica Argentina, 1, 16–18.

    Laurent, R. (1984) On some iguanid genera related to or previously confused with Liolaemus Wiegmann. Journal of Herpetology, 18 (4), 357–373.
    https://doi.org/10.2307/1564098

    Laurent, R. (1985) Segunda contribución al conocimiento de la estructura taxonómica del género Liolaemus Wiegmann (Iguanidae). Cuadernos de Herpetología, 1, 1–37.

    Lobo, F., Espinoza, R.E. & Quinteros, A.S. (2010) A critical review and systematic discussion of recent classification proposals for liolaemid lizards. Zootaxa, 2549, 1–30.

    MMA. (2016) Decreto Supremo Nº 16/2016 del Ministerio del Medio Ambiente, Chile. Available from: http://www.mma.gob.cl/clasificacionespecies/Anexo_duodecimo_proceso/DS_16-2016MMA_oficializa_12moRCE_DiarioOfi
    cial_1118600.pdf (accessed 11 May 2018)

    Navarro-Barón, J. (1991) Cariotipo de trece especies de lagartijas del noroeste argentino de los grupos Liolaemus, Eulaemus y Ortholaemus. Acta Zoológica Lilloana, 41, 225–230.

    Núñez, H. & Jaksic, F. (1992) Lista comentada de los reptiles terrestres de Chile continental. Boletín del Museo Nacional de Historia Natural de Chile, 43, 73–91.

    Núñez, H. & Navarro, J. (1992) Liolaemus rosenmanni, una nueva especie Chilena de lagartija relacionada al grupo 'ruibali'. Boletín del Museo Nacional de Historia Natural, 43, 55–62.

    Núñez, H. & Torres-Mura, J.C. (1992) Adiciones a la herpetofauna de Chile. Noticiario Mensual del Museo Nacional de Historia Natural, 322, 3–7.

    Núñez, H. & Yañez, J. (1983) Ctenoblepharis audituvelatus new species, a lizard from northern Chile (Reptilia Iguanidae). Copeia, 1983 (2), 454–457.
    https://doi.org/10.2307/14443

    Núñez, H. & Yáñez, J. (1984) Abas y Velosaura, nuevos géneros de lagartos iguanidae y proposiciones sistemáticas respecto de los géneros aliados (Reptilia: Squamata). Boletín del Museo Nacional de Historia Natural de Chile, 40, 91–95.

    Núñez, H., Mella, J. & Ruiz de Gamboa, M. (2017) Liolaemus audituvelatus. The IUCN Red List of Threatened Species 2017: e.T56050827A56050948.
    https://doi.org/10.2305/IUCN.UK.2017-2.RLTS.T56050827A56050948.en

    Núñez, H., Navarro, J., Garín, C., Pincheira-Donoso, D. & Meriggio, V. (2003) Phrynosaura manueli y Phrynosaura torresi, nuevas especies de lagartijas para el norte de Chile (Squamata: Sauria). Boletín del Museo Nacional de Historia Natural de Chile, 52, 67–88.

    Núñez, H., Navarro, J., Sufan, J. & Galaz, J.L. (1998) Distribución geográfica de Phrynosaura (Reptilia, Tropiduridae). Noticiario Mensual Museo Nacional de Historia Natural, 334, 11–14.

    Núñez, H., Yáñez, J. & Torres-Mura, J.C. (2012) Nuevas localidades para lagartijas del norte grande. Boletín del Museo Nacional de Historia Natural de Chile, 61, 177–183.

    Olave, M., Avila, L.J., Sites, J.W. Jr. & Morando, M. (2014) Multilocus phylogeny of the widely distributed South American lizard clade Eulaemus (Liolaemini, Liolaemus). Zoologica Scripta, 43 (4), 323–337.
    https://doi.org/10.1111/zsc.12053

    Pagel, M. & Meade, A. (2004) A Phylogenetic mixture model for detecting pattern heterogeneity in gene sequence or character-state data. Systematic Biology, 53, 571–581.
    https://doi.org/10.1080/10635150490468675

    Pagel, M. & Meade, A. (2005) Mixture models in phylogenetic inference. In: Gascuel, O. (Eds.), Mathematics of Evolution and Phylogeny. Oxford University Press, Oxford, pp. 121–142.

    Pagel, M. & Meade, A. (2008) Modelling heterotachy in phylogenetic inference by reversible-jump Markov chain Monte Carlo. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, 363, 3955–3964.
    https://doi.org/10.1098/rstb.2008.0178

    Pereyra, E.A. (1992) Nueva especie de lagarto andino: Liolaemus vallecurensis (Tropiduridae, Liolaeminae). Noticiario Mensual del Museo Nacional de Historia Natural, 321, 10–14.

    Philippi, R.A. (1860) Reise durch die Wüste Atacama, auf Befehl der chilenischen Regierung im Sommer 1853–1854. Eduard Anton, Halle, ix + 192 pp.

    Pincheira-Donoso, D. & Núñez, H. (2002) Situación taxonómica de Liolaemus ornatus Koslowsky, 1898 y Liolaemus pantherinus Pellegrin, 1909 (Sauria, Tropiduridae, Liolaeminae). Noticiario Mensual del Museo de Historia Natural de Chile, 350, 38–42.

    Pincheira-Donoso, D. & Núñez, H. (2005) Las especies chilenas del género Liolaemus Wiegmann 1834 (Iguania: Tropiduridae: Liolaeminae). Taxonomía, sistemática y evolución. Publicación Ocasional, Museo Nacional de Historia Natural, Chile, 59, 1–486.

    Pincheira-Donoso, D., Scolaro, J.A. & Sura, P. (2008) A monographic catalogue on the systematics and phylogeny of the South American iguanian lizard family Liolaemidae (Squamata, Iguania). Zootaxa, 1800, 1–85.

    Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
    https://doi.org/10.1093/molbev/msn083

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic barcode gap discovery for primary species delimitation. ‎Molecular Ecology, 21, 1864–1877.
    https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Rodríguez, F., Oliver, J.F., Marín, A. & Medina, J.R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.
    https://doi.org/10.1016/S0022-5193(05)80104-3

    Ruiz de Gamboa, M. & Ortiz-Zapata, J.C. (2016) Los poros precloacales como diferenciadores de sexo en Liolaemus (Squamata: Liolaemidae): el caso de L. jamesi (Boulenger, 1891). Gayana, 80 (1), 125–128.
    https://doi.org/10.4067/S0717-65382016000100012

    Schulte, J.A.II., Macey, J.R., Espinoza, R.E. & Larson, A. (2000) Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society, 69, 75–102.
    https://doi.org/10.1006/bijl.1999.0346

    Troncoso-Palacios, J. (2014) Revisión del estatus taxonómico de Liolaemus filiorum Pincheira-Donoso y Ramírez, 2005 (Iguania: Liolaemidae). Cuadernos de Herpetología, 28, 111–117.

    Uetz, P. & Hošek, J. (2016) The Reptile Database. Available from: http://www.reptile-database.org (accessed 12 May 2017)

    Valladares, J.P., Etheridge, R., Schulte, J., Manríquez, G. & Spotorno, A. (2002) Nueva especie de lagartija del norte de Chile, Liolaemus molinai (Reptilia: Liolaeminae). Revista Chilena de Historia Natural, 75 (3), 473–489.
    https://doi.org/10.4067/S0716-078X2002000300002

    Valladares, P., Marambio, Y., Ruiz de Gamboa, M. & Mella, J. (2016) Liolaemus manueli. The IUCN Red List of Threatened Species 2016: e.T56064748A56064844.
    https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T56064748A56064844.en

    Vidal, M., Ortiz, J.C., Marín, J.C., Poulin, E. & Moreno, P.I. (2012) Comparative phylogeography of two co-distributed species of lizards of the genus Liolaemus (Squamata: Tropiduridae) from Southern Chile. Amphibia-Reptilia, 33 (1), 55–67.
    https://doi.org/10.1163/156853811X622039

    Vidal, M.A., Soto, E. & Veloso, A. (2009) Biogeography of Chilean herpetofauna: distributional patterns of species richness and endemism. Amphibia-Reptilia, 30, 151–171.
    https://doi.org/10.1163/156853811X622039

    Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE. In: Lemey, P., Salemi, M. & Vandamme, A.-M. (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. 2nd Edition. Cambridge University Press, Cambridge, pp. 615–630.
    https://doi.org/10.1017/CBO9780511819049.022

    Xia, X. (2000) Data analysis in molecular biology and evolution. Boston: Kluwer Academic publishers, 296 pp.
    https://doi.org/10.1007/b113439

    Xia, X. (2013) DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 30, 1720–1728.
    https://doi.org/10.1093/molbev/mst064

    Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7.
    https://doi.org/10.1016/S1055-7903(02)00326-3

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