Abstract
Most of the lizards of the Liolaemus genus present precloacal pores in males, with few exceptions in species of the lineomaculatus and neuquensis groups, and in the elongatus-kriegi complex. The elongatus-kriegi complex, belonging to the Liolaemus (sensu stricto) subgenus, is composed of medium sized, saxicolous, viviparous and insectivorous or omnivorous lizards, distributed between the Andean and Patagonian zones of Chile and Argentina. We reviewed the taxonomic history of this group, and we describe two new species, Liolaemus carlosgarini, found in the vicinity of the Maule Lagoon, in the Maule Region, Chile, and Liolaemus riodamas, described from the population that was originally designated as Liolaemus cf. ceii, from Las Damas River, near the Termas del Flaco locality, in the Libertador Bernardo O’Higgins Region, thereby based on this research L. ceii is eliminated from the species belonging to Chile.
Both species have as a diagnostic character the absence of precloacal pores, and we suggest here their presumptive systematic relationships in Liolaemus. We analyzed ten species of Liolaemus, in order to perform a phylogenetic analysis based on external morphology, using mostly squamation and morphometric characters. The analysis was performed using PAUP, with the Maximum Parsimony criterion. In addition, through diaphanisation, we studied and described the osteology of the new species. We conclude that species lacking precloacal pores do not form a monophyletic group, and that constructing a phylogeny using only external morphology, at least for this group of reptiles, is insufficient to establish solid phyletic relationships. Other sort of characters should complement the morphological ones.
References
Abdala, C.S. (2007) Phylogeny of the boulengeri group (Iguania: Liolaemidae, Liolaemus) based on morphological and molecular characters. Zootaxa, 1538, 1–84.
Abdala, C.S., Quinteros, A.S., Scrocchi, G.S. & Stazzonelli, J.C. (2010) Three new species of the Liolaemus elongatus group (Squamata, Liolaemidae) from Argentina. Cuadernos de Herpetologia, 24, 93–109.
Avila, L.J., Morando, M., Perez, C.H.F. & Sites, J.W, Jr. (2004) Phylogenetic relationships of lizards of the Liolaemus petrophilus group (Squamata, Liolaemidae), with description of two new species from western Argentina. Herpetologica, 60, 187–203. http://dx.doi.org/10.1655/03-04
Avila, L.J., Morando, M., Perez, D.R. & Sites, J.W, Jr. (2010) A new species of the Liolaemus elongatus clade (Reptilia: Iguania: Liolaemini) from Cordillera del Viento, northwestern Patagonia, Neuquén, Argentina. Zootaxa, 2667, 28–42.
Avila, L.J., Perez, C.H.F., Medina C. D., Sites, J.W., Jr. & Morando, M. (2012) A new species of lizard of the Liolaemus elongatus clade (Reptilia: Iguania: Liolaemini) from Curi Leuvu River Valley, northern Patagonia, Neuquén, Argentina. Zootaxa, 3325, 35–52.
Avila, L.J., Perez, C.H.F. & Morando, M. (2003) A new species of Liolaemus (Squamata: Iguania: Liolaemidae) from northwestern Patagonia (Neuquen, Argentina). Herpetologica, 59, 532–543. http://dx.doi.org/10.1655/02-67
Breitman, M.F., Avila, L.J., Sites Jr., J.W. & Morando, M. (2011) Lizards from the end of the world: Phylogenetic relationships of the Liolaemus lineomaculatus section (Squamata: Iguania: Liolaemini). Molecular Phylogenetics and Evolution 59, 364–376. http://dx.doi.org/10.1016/j.ympev.2011.02.008
Cei, J.M. (1974) Revision of the Patagonian iguanids of the Liolaemus elongatus complex. Journal of Herpetology, 8, 219–229. http://dx.doi.org/10.2307/1563167
Cei, J.M. (1975) Herpetología patagónica. X. El conjunto evolutivo de Liolaemus elongatus: análisis serológico. Physis, Buenos Aires, 34, 203–208.
Cei, J.M. (1979) The Patagonian Herpetofauna. In W. E. Duellman (Ed.), The South American Herpetofauna: its Origin, Evolution, and Dispersal. Museum of Natural History, University of Kansas,Lawrence, Kansas, U.S.A. pp. 309–329.
Cei, J.M. (1986) Reptiles del centro, centro-oeste y sur de la Argentina. Herpetofauna de las zonas áridas y semiáridas. Museo Regionale di Scienze Naturali di Torino, Monografie 4, 528 pp.
Cei, J.M. & Ortiz, J.C. (1983) Descripción de una nueva especie de lagarto Liolaemus coeruleus n. sp. para Argentina. (Sauria, Iguanidae). Boletín de la Sociedad de Biología de Concepción, 54, 35–41.
Cei, J.M. & Videla, F. (2002) Singulares hallazgos evolutivos y taxonómicos en géneros de iguánidos relevantes de la herpetofauna andina y de zonas limítrofes. Multequina, Latin American Journal of Natural Resources, 11, 65–73.
Cei, J.M. & Videla, F. (2003) A new species of Liolaemus lacking precloacal pores in males from the Andean southeastern mountains of Mendoza Province, Argentina (Liolaemidae, Iguania, Lacertilia, Reptilia). Bollettino del Museo Regionale di Scienze Naturali di Torino, 20, 275–290.
Cruz, F.B., Fitzgerald, L.A., Espinoza, R.E. & Schulte II, J.A. (2005) The importance of phylogenetic scale in tests of Bergmann’s and Rapoport’s rules: lessons from a clade of South American lizards. Journal of Evolutionary Biology, 18, 1559–1574. http://dx.doi.org/10.1111/j.1420-9101.2005.00936.x
De Queiroz, K. (1987) Phylogenetic Systematics of Iguanine Lizards. University of California Publications 118, 203 pp.
Donoso-Barros, R. (1971) A new Liolaemus from Neuquén (Argentina). Herpetologica, 27, 49–51.
Donoso-Barros, R. & Cei, J.M. (1971) New lizards from the volcanic Patagonian plateau of Argentina. Journal of Herpetology, 5, 89–95. http://dx.doi.org/10.2307/1562730
Espinoza, R.E. & Lobo, F. (2003) Two new species of Liolaemus lizards from northwestern Argentina: speciation within the northern subclade of the elongatus group (Iguania: Liolaemidae). Herpetologica, 59, 89–105. http://dx.doi.org/10.1655/0018-0831(2003)059[0089:TNSOLL]2.0.CO;2
Espinoza, R.E., Lobo, F. & Cruz, F.B. (2000) Liolaemus heliodermis, a new lizard from northwestern Argentina with remarks on the content of the elongatus group (Iguania: Tropiduridae). Herpetologica, 56, 235–244.
Espinoza, R.E., Wiens, J.J. & Tracy, C.R. (2004) Recurrent evolution of herbivory in small, cold-climate lizards: Breaking the ecophysiological rules or reptilian herbivory. Proceedings of the National Academy of Sciences, USA, 101,16819–16824. http://dx.doi.org/10.1073/pnas.0401226101
Etheridge, R. (1995) Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the taxonomy of Liolaeminae (Reptilia:Squamata: Tropiduridae). American Museum Novitates, 3142, 1–34.
Etheridge, R. (2000) A review of lizards of the Liolaemus wiegmannii group (Squamata, Iguania, Tropiduridae), and a history of morphological change in the sand-dwelling species. Herpetological Monographs, 14, 293–352. http://dx.doi.org/10.2307/1467049
Etheridge, R & Espinoza, R.E. (2000) Taxonomy of the Liolaeminae (Squamata: Iguania: Tropiduridae) and a semiannotated bibliography. Smithsonian Herpetological Information Service, 126, 1–64.
Frost, D.R., Etheridge, R., Janies, D. & Titus, T.A. (2001) Total evidence, sequence alignment, evolution of Polychrotid lizards, and a reclassification of the Iguania (Squamata: Iguania). American Museum Novitates, 3343, 1–38. http://dx.doi.org/10.1206/0003-0082(2001)343<0001:TESAEO>2.0.CO;2
Hellmich, W. (1950) Die Eidechsen der Ausbeute Schröder (Gattung Liolaemus, Iguan.) (Beiträge zur Kenntnis der Herpetofauna Chiles XIII). Veröffentlichungen Zoologische Staatsammlung, München, 1, 129–194.
Hulse, A.C. (1979) A new Liolaemus (Sauria, Iguanidae) from the high Andes of Argentina, with ecological comments. Annals of the Carnegie Museum, 48, 203–209.
Koslowsky, J. (1896) Sobre algunos reptiles de patagonia y otras regiones argentinas. Revista del Museo de La Plata, 7,447–457.
Laurent, R.F. (1983) Contribución al conocimiento de la estructura taxonómica del género Liolaemus Wiegmann (Iguanidae). Boletín de la Asociación Herpetológica Argentina, 1, 15–18.
Laurent, R.F. (1985) Segunda contribución al conocimiento de la estructura taxonómica del género Liolaemus Wiegmann (Iguanidae). Cuadernos de Herpetología, 1, 1–37.
Laurent, R.F. (1995). A tentative arrangement of subgenera of the genus Liolaemus Wiegmann (Reptilia: Squamata: Tropiduridae). Bulletin of the Maryland Herpetological Society, 31, 10–14.
Lobo, F. (2001) A phylogenetic analysis of lizards of the Liolaemus chiliensis group (Iguania: Tropiduridae). Herpetological Journal, 11, 137–150.
Lobo, F. (2005) Las relaciones filogenéticas dentro del grupo chiliensis (Iguania: Liolaemidae: Liolaemus): sumando nuevos caracteres y taxones. Acta Zoológica Lilloana, 49, 67–89.
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.
Mahoney, R. (1973) Laboratory Techniques in Zoology. Second Edition. Butterworths & Co. London, 518 pp.
Morando, M., Avila, L.J., Baker, J. & Sites, J.W. (2004) Phylogeny and phylogeography of the Liolaemus darwinii complex (Squamata: Liolaemidae): evidence for introgression and incomplete lineage sorting. Evolution, 58, 842–861. http://dx.doi.org/10.1111/j.0014-3820.2004.tb00416.x
Morando, M., Avila, L.J. & Sites, J.W., Jr. (2003) Sampling strategies for delimiting species: genes, individuals, and populations in the Liolaemus elongatus–kriegi complex (Squamata: Liolaemidae) in Andean–Patagonian South America. Systematic Biology, 52, 159–185. http://dx.doi.org/10.1080/10635150390192717
Müller, L. & Hellmich, W. (1932) Beiträge zur Kenntnis der Herpetofauna Chiles. II. Neue Liolaemus Arten und Rassen aus den Hoch-Anden Chiles. Zoologischer Anzeiger, 97, 307–329.
Müller, L. & Hellmich, W. (1939) Liolaemus -Arten aus den westlichen Argentinien. III. Ueber Liolaemus kriegi, eine neue Liolaemus -Art aus des gegend der Lago Nahuel Huapi. Zoologischer Anzeiger, 127, 44–47.
Núñez, H. (2007) Liolaemus frassinettii, nueva especie de lagartija para los Altos de Cantillana, Región Metropolitana (Reptilia: Sauria). Boletín del Museo Nacional de Historia Natural de Chile, 57, 81–88.
Núñez, H. & Labra, A. (1985) Liolaemus curis, a new lizard from the Los Andes Range, central Chile. Copeia, 1985, 556–559. http://dx.doi.org/10.2307/1444743
Núñez, H., Navarro, J. & Loyola, J. (1991) Liolaemus maldonadae y Liolaemus cristiani, dos especies nuevas de lagartijas para Chile (Reptilia, Squamata). Boletín del Museo Nacional de Historia Natural de Chile, 42, 79–88.
Núñez, H. & Torres-Mura, J.C. (1992) Adiciones a la herpetofauna de Chile. Noticiario Mensual del Museo Nacional de Historia Natural de Chile, 322, 3–8.
Núñez, H., Veloso, A., Espejo, P., Veloso, C., Cortés & Araya, S. (2010) Nuevas especies de Phymaturus (grupo “palluma”) para la zona cordillerana central de Chile (Reptilia, Sauria, Liolaemidae). Boletín del Museo Nacional de Historia Natural de Chile, 59, 41–74.
Oelrich, T.M. (1956) The anatomy of the head of Ctenosaura pectinata. Miscellaneous publication of the Museum of Zoology, University of Michigan, 122 pp.
Peters, J.A. (1964) Dictionary of Herpetology. A brief and meaningful definitions of words and terms used in herpetology. Haffner Publishing Co. New York,392 pp.
Pincheira-Donoso, D. & Núñez, H. (2003) Liolaemus robertoi, una nueva especie de Los Andes del norte de Chile perteneciente al grupo ruibali (Iguania: Tropiduridae: Liolaeminae). Multequina, Latin American Journal of Natural Resources, 12, 1–15.
Pincheira-Donoso, D. & Núñez, H. (2005) Las especies chilenas del género Liolaemus (Iguania, Tropiduridae, Liolaeminae). Taxonomía, sistemática y evolución, Publicación Ocasional del Museo Nacional de Historia Natural de Chile, Santiago, 486 pp.
Pincheira-Donoso, D. & Scolaro, J.A. (2007) Iguanian species-richness in the Andes of boreal Patagonia: evidence for an additional new Liolaemus lizard from Argentina lacking precloacal glands (Iguania, Liolaeminae). Zootaxa, 1452, 55–68.
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.
Quinteros, A.S., Abdala, C.S., Díaz Gómez, J.M. & Scrocchi, G.J. (2008) Two new species of Liolaemus (Iguania: Liolaemidae) of Central West Argentina. South American Journal of Herpetology 3, 101–111. http://dx.doi.org/10.2994/1808-9798(2008)3[101:TNSOLI]2.0.CO;2
Schulte II, J.A., 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. http://dx.doi.org/10.1006/bijl.1999.0346
Scolaro, J.A., Videla, F., Puig, S. & Marcus, A. (2007) Diferencias morfológicas y status taxonómico de las especies simpátricas Liolaemus coeruleus y Liolaemus neuquensis (Reptilia: Iguania: Liolaemidae). Multequina, Latin American Journal of Natural Resources, 16, 53–63.
Troncoso-Palacios, J. & Lobo, F. (2012) A new species of Phymaturus (Iguania: Liolaemidae) of the palluma group from Central Chile. Cuadernos de Herpetología, 26, 69–78.
Torres Pérez, F., Méndez, M.A., Benavídez, E. Moreno, R.A., Lamborot, M., Palma, R.E. & Ortiz, J.C. (2009) Systematics and evolutionary relationships of the mountain lizard Liolaemus monticola (Liolaemini): how morphological and molecular evidence contributes to reveal hidden species diversity. Biological Journal of the Linnean Society, 96, 635–650. http://dx.doi.org/10.1111/j.1095-8312.2008.01140.x
Videla, F. & Cei, J.M. (1996) A new peculiar Liolaemus species of the “chiliensis” phyletic group from the volcanic Cordilleran landscapes of southern Mendoza Province, Argentina (Iguania, Lacertilia, Reptilia). Bollettino del Museo Regionale di Scienze Naturali di Torino, 14, 505–516.
Werner, F. (1907) In: Bürger, O. (Ed.), Estudios sobre reptiles chilenos. Anales Universidad de Chile, 121, 147–155.
Wiegmann, A.F.A. (1834) Herpetologica Mexicana seu descriptio amphibiorum Novae Hispaniae quae itineribus comitis de Sack, Ferdinandi Deppe et Chr. Guil. Schiede in Museum Zoologicum Berolinense pervenerunt. Pars prima, Saurorum species amplectens, adiecto Systematis Saurorum Prodromo, additisque multis in hunc amphibiorumordinem observationibus, C.G. Lüderitz, Berlin, 54 pp.
Young-Downey, A.R. (1998) Phylogenetic studies on Liolaemus (Sauria: Tropiduridae): an interpretation based on molecular data and a biochemical test of a biogeographic hypothesis. Unpublished Ph.D. Dissertation, University of Miami, Coral Gables, Florida. 85 pp