Thermal biology and locomotor performance in Phymaturus calcogaster: are Patagonian lizards vulnerable to climate change?

Behavioral and physiological traits of ectotherms are especially sensitive to fluctuations of environmental temperature. In particular, niche-specialist lizards are dependent on their physiological plasticity to adjust to changing environmental conditions. Lizards of the genus Phymaturus are viviparous, mainly herbivorous, and inhabit only rock promontories in the steppe environments of Patagonia and the Andes. Herein, we examine the vulnerability of the southernmost Phymaturus species to global warming: the endemic Phymaturus calcogaster, which lives in a mesic environment in eastern Patagonia. We studied body temperatures in the field (Tb ), preferred body temperatures in a thermogradient (Tpref ), the operative (Te ) and environmental temperatures, and the dependence of running performance on body temperature. P. calcogaster had a mean Tb (27.04°C) and a mean Te (31.15°C) both lower than their preferred temperature (Tpref = 36.61°C) and the optimal temperature for running performance (To = 37.13°C). Lizard activity seems to be restraint during the early afternoon due high environmental temperatures. However, both, the high safety margin and warming tolerance suggest that the expected increase in environmental temperatures due to global warming (IPCC report in 2018) would not threaten, but indeed enhance locomotor performance in this population.

Potential benefits from global warming to the thermal biology and locomotor performance of an endangered Patagonian lizard.

Global warming can significantly affect many aspects of the biology of animal species, including their thermal physiology and physiological performance. Thermal performance curves provide a heuristic model to evaluate the impacts of temperature on the ecophysiology of ectotherms. When integrated with other thermal biology parameters, they can be used to predict the impacts of climate change on individual fitness and population viability. In this study, we combine holistic measures of thermal physiology and the thermal sensitivity of locomotor performance with environmental temperatures measured at fine scale to estimate the vulnerability to global warming of the endangered Patagonian lizard Phymaturus tenebrosus. Our results indicate that this lizard exhibits its preferred temperatures and maximum locomotor performance at higher temperatures than the mean temperature it currently experiences in its habitat. In addition, it exhibits a low effectiveness of thermoregulation, being a poor thermoregulator. In view of the results obtained, we suggest that the climatic conditions of Patagonia may be advantageous for P. tenebrosus to survive future global warming, since its thermal physiology and locomotor performance may improve under increasing in environmental temperatures in its habitat.

A New Species of Lizard Endemic to Sierra de Fiambalá, Northwestern Argentina (Iguania: Liolaemidae: Phymaturus). Integrated Taxonomy Using Morphology and DNA Sequences: Reporting Variation Within the antofagastensis Lineage.

The northernmost distributed group of lizards belonging to Phymaturus occurs in rocky outcrops of the Puna region between 3600-4200 m in Argentina. In a recent phylogenetic study based on morphological and genetic information, the monophyly of this small lineage was corroborated. This group is formed by Phymaturus antofagastensis, P. laurenti, P. denotatus, P. mallimaccii and a population of uncertain taxonomic status until the present study. After obtaining new samples and observations, we described a new species belonging to this lineage that is known only from Sierra de Fiambalá, being the species of Phymaturus living at the highest elevation ever recorded (4500 m). Males have a homogeneous yellow dorsum and lack melanic coloration over their heads, a phenomenon found in males of most species of the palluma group. We provide a detailed diagnosis, including characters from the squamation, coloration and significant differences found among continuous characters (ANOVA). Furthermore, we present genetic distances among members of the mallimaccii subclade based on sequences of the cytb marker. We provide color photos showing pattern variation of males and females. We reanalyze the phylogenetic relationships within the entire palluma group and update info on all members of the antofagastensis lineage based on new samples and make a better supported hypothesis. We also evaluate the phylogenetic position of the new taxon.

How mountains shape biodiversity: The role of the Andes in biogeography, diversification, and reproductive biology in South America's most species-rich lizard radiation (Squamata: Liolaemidae).

Testing hypotheses on drivers of clade evolution and trait diversification provides insight into many aspects of evolutionary biology. Often, studies investigate only intrinsic biological properties of organisms as the causes of diversity, however, extrinsic properties of a clade's environment, particularly geological history, may also offer compelling explanations. The Andes are a young mountain chain known to have shaped many aspects of climate and diversity of South America. The Liolaemidae are a radiation of South American reptiles with over 300 species found across most biomes and with similar numbers of egg-laying and live-bearing species. Using the most complete dated phylogeny of the family, we tested the role of Andean uplift in biogeography, diversification patterns, and parity mode of the Liolaemidae. We find that the Andes promoted lineage diversification and acted as a species pump into surrounding biomes. We also find strong support for the role of Andean uplift in boosting the species diversity of these lizards via allopatric fragmentation. Finally, we find repeated shifts in parity mode associated with changing thermal niches, with live-bearing favored in cold climates and egg-laying favored in warm climates. Importantly, we find evidence for possible reversals to oviparity, an evolutionary transition believed to be extremely rare.

Effect of temperature on the locomotor performance of species in a lizard assemblage in the Puna region of Argentina.

Locomotion is relevant to the ecology of reptiles because of its presumed influence on an organism's Darwinian fitness. Moreover, in ectothermic species, physiological performance capacity is affected by body temperature. We analyzed two components of locomotor performance in three species of lizards, Phymaturus extrilidus, Liolaemus parvus, and Liolaemus ruibali, in the Puna environment of Argentina. First, we estimated the thermal sensitivity of locomotion by measuring sprint speed at four different body temperatures. We included two measures of sprint speed: initial velocity and long sprint for sustained runs. Based on these data, we calculated the optimal temperature for performance and the optimal performance breadth. We also estimated endurance capacity at a single temperature. Maximum sprint speed for L. parvus was greater than L. ruibali and P. extrilidus in both initial velocity and long sprint. In contrast, L. parvus exhibited lower levels of endurance than L. ruibali and P. extrilidus. However, endurance in L. ruibali exceeded that of P. extrilidus. The species differed in the optimal temperature for the initial velocity with the lowest for L. ruibali (31.8 °C) followed by P. extrilidus (33.25 °C) and then L. parvus (36.25 °C). The optimal temperature for long sprint varied between 32 and 36 °C for all species. We found that all species attained maximum performance at body temperatures commonly experienced during daily activity, which was higher than the thermal quality of the environment. We found evidence for thermal sensitivity in locomotor performance in these species. However, we also show that the broad thermal breadth of performance suggests that the lizards are capable of sustaining near optimal levels of locomotor performance at ambient temperatures that would appear to be suboptimal. Thus, this lizard assemblage is capable of coping with the highly variable climatic conditions in the Puna region of Argentina.

An updated phylogeny and morphological study of the Phymaturus vociferator clade (Iguania: Liolaemidae).

Species delimitation in Phymaturus has been a difficult task due to the highly conserved morphological and ecological features present in this genus. Almost all species of Phymaturus have been described without DNA data or lacking statistical analyses which makes even more difficult to compare species. Although two molecular phylogenetic studies have been recently published, here we provide the first multilocus phylogenetic reconstruction including all Chilean species, with samples from all type localities and some previously unsampled populations. We also estimate pairwise distances among the Chilean species of Phymaturus (P. vociferator and P. mallimaccii clades) and compare our results with the P. payuniae clade, where previous studies have used multiple lines of evidence. Additionally, we performed univariate and multivariate morphological analyses and skeletal comparisons (clavicle) for the species of the P. vociferator clade. As a result of this integrative approach, we describe a new species.

Macroevolutionary diversification with limited niche disparity in a species-rich lineage of cold-climate lizards.

BACKGROUND: Life diversifies via adaptive radiation when natural selection drives the evolution of ecologically distinct species mediated by their access to novel niche space, or via non-adaptive radiation when new species diversify while retaining ancestral niches. However, while cases of adaptive radiation are widely documented, examples of non-adaptively radiating lineages remain rarely observed. A prolific cold-climate lizard radiation from South America (Phymaturus), sister to a hyper-diverse adaptive radiation (Liolaemus), has extensively diversified phylogenetically and geographically, but with exceptionally minimal ecological and life-history diversification. This lineage, therefore, may offer unique opportunities to investigate the non-adaptive basis of diversification, and in combination with Liolaemus, to cover the whole spectrum of modes of diversification predicted by theory, from adaptive to non-adaptive. Using phylogenetic macroevolutionary modelling performed on a newly created 58-species molecular tree, we establish the tempo and mode of diversification in the Phymaturus radiation. RESULTS: Lineage accumulation in Phymaturus opposes a density-dependent (or 'niche-filling') process of diversification. Concurrently, we found that body size diversification is better described by an Ornstein-Uhlenbeck evolutionary model, suggesting stabilizing selection as the mechanism underlying niche conservatism (i.e., maintaining two fundamental size peaks), and which has predominantly evolved around two major adaptive peaks on a 'Simpsonian' adaptive landscape. CONCLUSIONS: Lineage diversification of the Phymaturus genus does not conform to an adaptive radiation, as it is characterised by a constant rate of species accumulation during the clade's history. Their strict habitat requirements (rocky outcrops), predominantly invariant herbivory, and especially the constant viviparous reproduction across species have likely limited their opportunities for adaptive diversifications throughout novel environments. This mode of diversification contrasts dramatically with its sister lineage Liolaemus, which geographically overlaps with Phymaturus, but exploits all possible microhabitats in these and other bioclimatic areas. Our study contributes importantly to consolidate these lizards (liolaemids) as promising model systems to investigate the entire spectrum of modes of species formations, from the adaptive to the non-adaptive extremes of the continuum.

Slow life histories in lizards living in the highlands of the Andes Mountains.

In the highlands of the Andes, lizards must balance precisely the allocation of energy for growth and reproduction to ensure their survival. We studied the individuals' age, growth rates, age at sexual maturity, and maximum life span of the viviparous lizard Phymaturus antofagastensis, endemic of cold and harsh environments at high altitudes in the Andes Mountains of Catamarca province, Argentina. We also estimated key life history parameters like reproductive effort, lifetime reproductive effort, net reproductive rate, and relative reproductive time in P. antofagastensis as well as in other Phymaturus to compare the interplay among growth, maintenance, and reproduction in species that live across a latitudinal and altitudinal gradient. We found that females and males of P. antofagastensis mature late in life, at 6-7 years old, respectively, and some individuals reached 20 years of age. Adult females showed higher specific growth rates than males and an adult life span of 9 years which, due to their biennial reproduction, results in an estimated production of only four litters in life. This species exhibits one of the highest lifetime reproductive efforts described for lizards. Our results indicate the existence of a tradeoff between the number of reproductive events throughout life and reproductive effort devoted to each event in Phymaturus, related to the phylogenetic group. The palluma group shows low reproductive effort but high number of reproductive events throughout their lives, whereas the patagonicus group shows high reproductive efforts in low number of reproductive events.

Thermal physiology of three sympatric and syntopic Liolaemidae lizards in cold and arid environments of Patagonia (Argentina).

The thermal physiology determines the whole biology of ectotherm organisms, by limiting their acquisition and allocation of resources. Herein, we aim to add knowledge on how different species use the thermal resources when they coexist in a habitat, studying the thermal physiology of three sympatric and syntopic liolaemid lizards, Phymaturus querque, Phymaturus zapalensis, and Liolaemus elongatus during the summer season. We measured the body temperatures at capture places, the operative microenvironmental temperatures in the field, and the preferred body temperature in an experimental thermal gradient in the laboratory. We found that the three species are thermoregulators, selecting cooler thermal microenvironments than the ones expected by chance, and even cooler than the temperatures they selected in a laboratory environment. Liolaemus elongatus is a more efficient thermoregulator (E = 0.671) than the two Phymaturus species, P. querque (E = 0.441) and P. zapalensis (E = 0.471), which are moderate thermoregulators and, apparently, specialists in finding specific types of shelters, since they seem to select certain types of rock crevices. Herein, we found that during the summer season, although individuals have access to warm microenvironments, they spend time on cool refuges, probably to prevent overheating. This highlights the importance of an adequate spatial distribution of operative temperatures (T e), more than just a mere availability of appropriate temperatures.

A morphology-based phylogeny of Phymaturus (Iguania: Liolaemidae) with the description of four new species from Argentina

Phylogenetic relationships within the liolaemid lizard genus Phymaturus were studied using parsimony analysis of morphological data. The data set includes 133 characters: 28 described in the literature as apomorphies of the three genera of Liolaemidae (Ctenoblepharys, Liolaemus, and Phymaturus), 21 published characters of allozymes and karyology, 53 characters taken from external morphology across all terminals of Phymaturus, and 31 from the skeletal anatomy. This data set includes representatives of 10 of the 12 species currently recognized in the literature plus twelve other terminals considered in this study and representing independent lineages assigned to patagonicus or palluma. Four of these terminals are described in the present study as new species, one belonging to the palluma group and the other three to the patagonicus group. We performed four analyses using different methods of coding binary polymorphic characters, and a new method for treating continuous characters. The traditional division of the genus in two groups is not supported here, with the patagonicus group resulting paraphyletic in some of the analyses. The palluma group is monophyletic and supported by many characters. A majority rule consensus tree of all runs recovers a reasonably well-resolved topology of the group. All analyses recovered a northern subclade within the palluma group, formed by species distributed in Argentina from northern of San Juan province (north to 30 degrees of latitude). In this analysis palluma from El Planchón (Chile) was found to be more closely related to this northern subclade than any other "palluma" form.

Estudaram-se as relações dentro do gênero Phymaturus da familia Liolaemidae, usando análise de parsimônia de uma matriz formada principalmente por dados morfológicos. A matriz inclui 133 caracteres: 28 descritos na literatura como apomorfias dos três gêneros de Liolaemidae (Ctenoblepharys, Liolaemus e Phymaturus), 21 caracteres de alozimas e cariologia, 53 caracteres de morfologia externa e 31 do esqueleto, de todos os terminais de Phymaturus. A matriz inclui representantes de dez das doze espécies reconhecidas na literatura, e outros 12 terminais que neste estudo se consideram linhagens independentes e identificadas como P. patagonicus ou P. palluma na literatura prévia e nas coleções. Quatro destes terminais são descritos neste trabalho como espécies novas, uma pertencente ao grupo de P. palluma e outras três ao grupo de P. patagonicus. Realizaram-se quatro análises usando quatro métodos diferentes para codificar binariamente caracteres polimórficos, e um novo método para codificar os caracteres contínuos. A divisão tradicional do gênero em dois grupos não é apoiada pelo presente estudo, o grupo de P. patagonicus é parafilético em parte da análise. O grupo de P. palluma é monofilético e se sustenta por vários caracteres, as árvores de consenso por maioria, de todas as análises, mostraram com exceção de um par de politomías, uma topologia do grupo bem resolvida. Dentro do grupo de P. palluma, encontra-se um subclado formado por espécies distribuídas no norte da Argentina desde o norte da província de San Juan (ao norte dos 30° de latitude). Nesta análise, o P. palluma de El Planchón (Chile), relaciona-se mais com este subclado do norte que com qualquer outra forma de "P. palluma".

A morphology-based phylogeny of Phymaturus (Iguania: Liolaemidae) with the description of four new species from Argentina

Phylogenetic relationships within the liolaemid lizard genus Phymaturus were studied using parsimony analysis of morphological data. The data set includes 133 characters: 28 described in the literature as apomorphies of the three genera of Liolaemidae (Ctenoblepharys, Liolaemus, and Phymaturus), 21 published characters of allozymes and karyology, 53 characters taken from external morphology across all terminals of Phymaturus, and 31 from the skeletal anatomy. This data set includes representatives of 10 of the 12 species currently recognized in the literature plus twelve other terminals considered in this study and representing independent lineages assigned to patagonicus or palluma. Four of these terminals are described in the present study as new species, one belonging to the palluma group and the other three to the patagonicus group. We performed four analyses using different methods of coding binary polymorphic characters, and a new method for treating continuous characters. The traditional division of the genus in two groups is not supported here, with the patagonicus group resulting paraphyletic in some of the analyses. The palluma group is monophyletic and supported by many characters. A majority rule consensus tree of all runs recovers a reasonably well-resolved topology of the group. All analyses recovered a northern subclade within the palluma group, formed by species distributed in Argentina from northern of San Juan province (north to 30 degrees of latitude). In this analysis palluma from El Planchón (Chile) was found to be more closely related to this northern subclade than any other "palluma" form.

Estudaram-se as relações dentro do gênero Phymaturus da familia Liolaemidae, usando análise de parsimônia de uma matriz formada principalmente por dados morfológicos. A matriz inclui 133 caracteres: 28 descritos na literatura como apomorfias dos três gêneros de Liolaemidae (Ctenoblepharys, Liolaemus e Phymaturus), 21 caracteres de alozimas e cariologia, 53 caracteres de morfologia externa e 31 do esqueleto, de todos os terminais de Phymaturus. A matriz inclui representantes de dez das doze espécies reconhecidas na literatura, e outros 12 terminais que neste estudo se consideram linhagens independentes e identificadas como P. patagonicus ou P. palluma na literatura prévia e nas coleções. Quatro destes terminais são descritos neste trabalho como espécies novas, uma pertencente ao grupo de P. palluma e outras três ao grupo de P. patagonicus. Realizaram-se quatro análises usando quatro métodos diferentes para codificar binariamente caracteres polimórficos, e um novo método para codificar os caracteres contínuos. A divisão tradicional do gênero em dois grupos não é apoiada pelo presente estudo, o grupo de P. patagonicus é parafilético em parte da análise. O grupo de P. palluma é monofilético e se sustenta por vários caracteres, as árvores de consenso por maioria, de todas as análises, mostraram com exceção de um par de politomías, uma topologia do grupo bem resolvida. Dentro do grupo de P. palluma, encontra-se um subclado formado por espécies distribuídas no norte da Argentina desde o norte da província de San Juan (ao norte dos 30° de latitude). Nesta análise, o P. palluma de El Planchón (Chile), relaciona-se mais com este subclado do norte que com qualquer outra forma de "P. palluma".