Multiple Sources of Evidence Reveal That Liolaemus cinereus Monguillot et al., 2006 is a Synonym of L. montanezi Cabrera and Monguillot, 2006

Esquerré D., Keogh J.S., Demangel D., Morando M., Avila L.J., Sites J.W., Ferri-Yáñez F., Leaché A.D.

Abstract Understanding the factors that cause heterogeneity among gene trees can increase the accuracy of species trees. Discordant signals across the genome are commonly produced by incomplete lineage sorting (ILS) and introgression, which in turn can result in reticulate evolution. Species tree inference using the multispecies coalescent is designed to deal with ILS and is robust to low levels of introgression, but extensive introgression violates the fundamental assumption that relationships are strictly bifurcating. In this study, we explore the phylogenomics of the iconic Liolaemus subgenus of South American lizards, a group of over 100 species mostly distributed in and around the Andes mountains. Using mitochondrial DNA (mtDNA) and genome-wide restriction site-associated DNA sequencing (RADseq; nDNA hereafter), we inferred a time-calibrated mtDNA gene tree, nDNA species trees, and phylogenetic networks. We found high levels of discordance between mtDNA and nDNA, which we attribute in part to extensive ILS resulting from rapid diversification. These data also reveal extensive and deep introgression, which combined with rapid diversification, explain the high level of phylogenetic discordance. We discuss these findings in the context of Andean orogeny and glacial cycles that fragmented, expanded, and contracted species distributions. Finally, we use the new phylogeny to resolve long-standing taxonomic issues in one of the most studied lizard groups in the New World.[Andes; ddRADSeq; introgression; lizards; mtDNA; reptiles; SNPs.]

Laspiur A., Santos J.C., Medina S.M., Pizarro J.E., Sanabria E.A., Sinervo B., Ibargüengoytía N.R.

Given the rapid loss of biodiversity as consequence of climate change, greater knowledge of ecophysiological and natural history traits are crucial to determine which environmental factors induce stress and drive the decline of threatened species. Liolaemus montanezi (Liolaemidae), a xeric-adapted lizard occurring only in a small geographic range in west-central Argentina, constitutes an excellent model for studies on the threats of climate change on such microendemic species. We describe field data on activity patterns, use of microhabitat, behavioral thermoregulation, and physiology to produce species distribution models (SDMs) based on climate and ecophysiological data. Liolaemus montanezi inhabits a thermally harsh environment which remarkably impacts their activity and thermoregulation. The species shows a daily bimodal pattern of activity and mostly occupies shaded microenvironments. Although the individuals thermoregulate at body temperatures below their thermal preference they avoid high-temperature microenvironments probably to avoid overheating. The population currently persists because of the important role of the habitat physiognomy and not because of niche tracking, seemingly prevented by major rivers that form boundaries of their geographic range. We found evidence of habitat opportunities in the current range and adjacent areas that will likely remain suitable to the year 2070, reinforcing the relevance of the river floodplain for the species’ avoidance of extinction.

Ruiz S., Quipildor M., Ruiz-Monachesi M.R., Escalante L., Valdecantos S., Lobo F.

Andean orogeny is one of the main factors that promoted the diversification of many groups of animals. Among them are the lizards of the Liolaemidae family and within this, Liolaemus is the genus with the most described species up to date, with approximately 277 species. One of the groups within the genus is the Liolaemus ornatus group, distributed in the south of Central Andes mountain chain. In this work, we describe a new species belonging to the L. ornatus group, using an integrative approach, analyzing both morphological (lepidosis, morphometric, coloration and hemipenes characters) and molecular evidence. We made a divergence analysis of the representatives of the L. ornatus group. Furthermore, we correlated the ages of the geological events with the distribution areas for the L. ornatus group. This newly described species shows character states (morphological and molecular) that allow its clear distinction from the other members of the L. ornatus group, as well as from the rest of Liolaemus . The divergence analysis places the new species in the L. ornatus group and allows us to infer the successive geological events that served as physical barriers for the diversification of the group, besides explaining the current distribution of the group.

Sánchez K.I., Avila L.J., Sites Jr. J.W., Morando M.

• We use an integrative approach to test species limits in Patagonian lizards. • We found support for a candidate species. • We detected genome-wide signs of hybridization. • More data is needed to assess the extent of hybridization and taxonomic implications. Recent conceptual and methodological advances have enabled an increasing number of studies to address the problem of species delimitation in a comprehensive manner. This is of particular interest in cases of species whose divergence times are recent and/or effective population sizes are large, where the conclusions obtained from a single source of evidence may lead to erroneous estimations of true species numbers or incorrect assignment of individuals to species. Iguanian lizards of the Liolaemus kingii group (13 species) comprise an important component of the endemic fauna of Patagonia. The southernmost species of this group (namely L. baguali , L. escarchadosi , L. sarmientoi , and L. tari ) show widely overlapping distributions across southern Patagonia, also, their phylogenetic relationships are ambiguous and species boundaries have not been explicitly tested. Here we use a comprehensive approach to assess species limits through the use of molecular and morphological information (mitochondrial cytb , nuclear sequences collected by ddRADseq, and linear, meristic and landmark-based morphometrics). We found support for the current taxonomy given that the different analyses recognized the nominal species (4 entities), also a candidate species was supported by mitochondrial and morphological data. In addition, we detected signs of admixture between some of the species. Our results indicate that the L. kingii group can serve as a model system in studies of diversification accompanied by hybridization in nature, which in turn might have been promoted by past climatic oscillations and generalist morphologies. We emphasize the importance of using multiple lines of evidence in order to solve evolutionary stories, and minimizing potential erroneous results that may arise when relying on a single source of information.

AVILA L.J., VRDOLJAK J.E., MEDINA C.D., MASSINI J.G., PEREZ C.H., SITES J.W., MORANDO M.

A new species of the Liolaemus capillitas clade is described. Liolaemus galactostictos sp. nov. differs from other members of its group by a combination of morphological and molecular traits, in particular its black dorsal coloration pattern not found in any other Liolaemus species. Liolaemus galactostictos sp. nov. is only known from its type locality. This new species is found in rocky fields surrounded by grasslands on the top of the Velasco Mountains, a ¨sky island environment¨, in northwestern Argentina. As well as other members of its clade this species seems to be strictly saxicolous, viviparous and feeds on insects. 

Abdala C.S., Paz M.M., Semhan R.V., García N., Aguilar-Kirigin A.J., Farías M.E., Valladares P., Poblete R.G., Quipildor M.A., Valdes J., Langstroth R.

The known diversity of the genus Liolaemus continues to increase, principally due to its great degree of endemism, the increasing number of researchers working on it, and advances in the taxonomic ...

Simón Abdala C., Quiróz A.J., Gutiérrez Poblete R.C., Luque-Fernández C., Huamaní-Valderrama L., Villegas Paredes L.

El género Liolaemus presenta una gran diversidad entre los tetrápodos actuales, al punto de corresponder al segundo género con mayor número de especies válidas descritas del infraorden Iguania. En este trabajo, se describe una nueva especie de lagartija arenícola perteneciente al subgénero Eulaemus, grupo de Liolaemus montanus, procedente de las lomas costeras de Quilca, La Chira y Ocoña, todos en la provincia de Camaná, departamento de Arequipa, Perú. Para determinar el estatus taxonómico de esta nueva especie, analizamos los caracteres morfológicos, moleculares y geográficos. Los caracteres morfológicos permitieron la caracterización y diagnóstico de la nueva especie, los moleculares fueron utilizados para realizar una inferencia bayesiana y los geográficos para determinar potenciales áreas de distribución. Este reptil se diferencia de las otras especies del grupo Liolaemus montanus en su tamaño pequeño a mediano, su conjunto de caracteres morfológicos, folidosis y patrón de coloración: es la única especie del género donde los machos tienen un patrón de manchas laterales de forma redondeada con borde oscuro e interior verde desde las axilas hasta la mitad del cuerpo. Del mismo modo, los resultados filogenéticos moleculares realizados con el gen Cyt-b indican que no tiene relación directa con las especies fenéticamente similares descritas para el grupo. Sin embargo, existe una relación con poblaciones geográficamente cercanas que permanecen taxonómicamente innominadas. Finalmente, se determinó que esta lagartija tiene un endemismo muy marcado y sus poblaciones son poco abundantes.

Abdala C.S., Aguilar-Kirigin A.J., Semhan R.V., Bulacios Arroyo A.L., Valdes J., Paz M.M., Gutiérrez Poblete R., Valladares Faundez P., Langstroth R., Aparicio J.

The Liolaemus montanus group is a diverse group of lizards that ranges from central Peru to southwestern Mendoza, Argentina, including much of the Plurinational State of Bolivia (“Bolivia”) and Chile. The species of this group mainly inhabit high elevation areas with cold temperatures. In the last years, several species of this group have been described, mostly in Argentina and Chile. In Bolivia, there are at least thirteen valid species belonging to the L. montanus group. In this study, we describe a new species of the L. montanus group with a marked endemism in the Cordillera de Sama of the Tarija Department, Bolivia, and a combination of unique character states that allows its formal description as a new species. The phylogenetic relationships based on analysis of 159 morphological characters suggest that it belongs to the L. montanus group, and that it is closest to Liolaemus pulcherrimus, which is found allopatrically in a small area of the Jujuy Province, Argentina. The multivariate analyses of 66 morphological characters support the phylogenetic relationships. Statistical analyses of inter-species comparisons of morphological characters are not considered the only methods due to the non-independence of some characters states among species; thus, a phylogenetic analysis is recommended. The detailed revision of specimens of the L. montanus group held in the collections of Bolivia is filling major geographic gaps and improving our understanding of the phylogenetic and biogeographic relationships of this widely distributed group of South American lizards.

Langstroth R., Garcia N., Aparicio J., Santa Cruz R., Portelli S., Valdés J., Valladares Faundez P., Gutiérrez Poblete R., Aguilar-Kirigin A.J., Laspiur A., Ruiz-Monachesi M.R., Paz M.M., Schulte J., Bulacios Arroyo A.L., Semhan R.V., et. al.

AbstractThe South American lizard genus Liolaemus comprises > 260 species, of which > 60 are recognized as members of the Liolaemus montanus group, distributed throughout the Andes in central Peru, Bolivia, Chile and central Argentina. Despite its great morphological diversity and complex taxonomic history, a robust phylogenetic estimate is still lacking for this group. Here, we study the morphological and molecular diversity of the L. montanus group and present the most complete quantitative phylogenetic hypothesis for the group to date. Our phylogeny includes 103 terminal taxa, of which 91 are members of the L. montanus group (58 are assigned to available species and 33 are of uncertain taxonomic status). Our matrix includes 306 morphological and ecological characters and 3057 molecular characters. Morphological characters include 48 continuous and 258 discrete characters, of which 70% (216) are new to the literature. The molecular characters represent five mitochondrial markers. We performed three analyses: a morphology-only matrix, a molecular-only matrix and a matrix including both morphological and molecular characters (total evidence hypothesis). Our total evidence hypothesis recovered the L. montanus group as monophyletic and included ≥ 12 major clades, revealing an unexpectedly complex phylogeny.

Abdala C.S., Ruiz-Monachesi M.R., Quinteros A.S.

AbstractWe redescribe Liolaemus bibronii and describe three new species of Liolaemus, a genus of lizards distributed across South America. These species belong to the L. alticolor–bibronii group, which are included in the subgenus Liolaemus s.s. Liolaemus bibronii was previously proposed as a species complex, but many populations initially assigned to this complex were described as valid species. The three new species described here were populations denominated under L. bibronii. In order to validate the new species, we apply an integrative approach, including molecular and morphological evidence. Also, we perform phylogenetic analyses applying parsimony and Bayesian inference. The three new species described here show a set of character states that allow them to be distinguished from L. bibronii, from each other and from all other species of Liolaemus. Our phylogenies show that the newly described species are more related to other species than to L. bibronii. With this study, we are closer to solving the taxonomic puzzle that L. bibronii represents.

Aguilar-Puntriano C., Ramírez C., Castillo E., Mendoza A., Vargas V.J., Sites J.W.

Three new species of Liolaemus belonging to the L. montanus group are described from Perú. Two new species are restricted to the Ica and Moquegua departments on the Pacific coast, and one new species is only known from an isolated highland in Ayacucho department. These three new species differ from closely related species in their coloration patterns and head shape. We comment on the conservation issues of the new species and other Peruvian species of the L. montanus group.

Ruiz S., Quipildor M., Bulacios Arroyo A., Chafrat P., Abdala C.

DE GAMBOA M.R., CORREA C., MARAMBIO-ALFARO Y., RIVEROS-RIFFO E., ORTIZ J.C.

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. 

Medina C.D., Avila L.J., Sites J.W., Santos J., Morando M.

We present different approaches to a multi-locus phylogeny for the Liolaemus elongatus-kriegi group, including almost all species and recognized lineages. We sequenced two mitochondrial and five nuclear gene regions for 123 individuals from 35 taxa, and compared relationships resolved from concatenated and species tree methods. The L. elongatus-kriegi group was inferred as monophyletic in three of the five analyses (concatenated mitochondrial, concatenated mitochondrial + nuclear gene trees, and SVD quartet species tree). The mitochondrial gene tree resolved four haploclades, three corresponding to the previously recognized complexes: L. elongatus, L. kriegi and L. petrophilus complexes, and the L. punmahuida group. The BEAST species tree approach included the L. punmahuida group within the L. kriegi complex, but the SVD quartet method placed it as sister to the L. elongatus-kriegi group. BEAST inferred species of the L. elongatus and L. petrophilus complexes as one clade, while SVDquartet inferred these two complexes as monophyletic (although with no statistical support for the L. petrophilus complex). The species tree approach also included the L. punmahuida group as part of the L. elongatus-kriegi group. Our study provides detailed multilocus phylogenetic hypotheses for the L. elongatus-kriegi group, and we discuss possible reasons for differences in the concatenation and species tree methods.

Portelli S.N., Quinteros A.S.

The genusLiolaemuscomprises more than 260 species and can be divided in two subgenera:EulaemusandLiolaemus sensu stricto. In this paper, we present a phylogenetic analysis, divergence times, and ancestral distribution ranges of theLiolaemus alticolor-bibroniigroup (Liolaemus sensu strictosubgenus). We inferred a total evidence phylogeny combining molecular (Cytband12Sgenes) and morphological characters using Maximum Parsimony and Bayesian Inference. Divergence times were calculated using Bayesian MCMC with an uncorrelated lognormal distributed relaxed clock, calibrated with a fossil record. Ancestral ranges were estimated using the Dispersal-Extinction-Cladogenesis (DEC-Lagrange). Effects of somea prioriparameters of DEC were also tested. Distribution ranged from central Perú to southern Argentina, including areas at sea level up to the high Andes. TheL. alticolor-bibroniigroup was recovered as monophyletic, formed by two clades:L. walkeriandL. gracilis, the latter can be split in two groups. Additionally, many species candidates were recognized. We estimate that theL. alticolor-bibroniigroup diversified 14.5 Myr ago, during the Middle Miocene. Our results suggest that the ancestor of theLiolaemus alticolor-bibroniigroup was distributed in a wide area including Patagonia and Puna highlands. The speciation pattern follows the South-North Diversification Hypothesis, following the Andean uplift.