Podarcis Muralis Research Articles

Epistatic interactions between pterin and carotenoid genes modulate intra-morph color variation in a lizard.

Color polymorphisms have become a major topic in evolutionary biology and substantial efforts have been devoted to the understanding of the mechanisms responsible for originating such colorful systems. Within-morph continuous variation, on the other hand, has been neglected in most of the studies. Here, we combine spectrophotometric/visual modeling and genetic data to study the mechanisms promoting continuous variation within categorical color morphs of Podarcis muralis. Our results suggest that intra-morph variability in the pterin-based orange morph is greater compared to white and yellow morphs. We also show that continuous variation within the orange morph is partially discriminable by conspecifics. Genotyping results indicate that allelic variants at the BCO2 locus (responsible for deposition of yellow carotenoids) contribute to generate continuous variation in orange individuals. However, other intrinsic and/or extrinsic mechanisms, such as body size, might be involved, opening a new avenue for future research on the drivers of continuous variation within-morphs.

Immunolocalization of Cell Adhesion Molecules during tail regeneration in the lizard Podarcis muralis indicates coordinated control of epithelial differentiation

AbstractImmunolocalization of cell adhesion molecules during tail regeneration in the lizard Podarcis muralis indicates coordinated control of epithelial differentiation. Acta Zoologica (Stockolm). Lizard epidermis is formed by alternating layers of hard corneous beta‐layers and softer and pliable alpha‐layers. After tail amputation in the lizard Podarcis muralis, the tail regenerates within a month forming neogenic scales. The differentiation of beta‐ and alpha‐layers in the epidermis has been studied by immunofluorescence detection of cell adhesion molecules. Initially, the thick wound epidermis shows high content in L‐CAM and N‐CAM in comparison with normal epidermis, including pre‐corneous layers where labelling is intense in the cytoplasm and along the keratinocyte perimeter. L‐ and N‐CAMs are also observed in the regenerating ependyma and N‐CAM in mesenchymal cells of blastema. The apical regenerating (wound) epidermis often shows nuclear localization in basal layers, especially for E‐cadherin, perhaps indicating epithelial–mesenchymal transition. Sections of regenerating scales show the typical renewal phase of the epidermis, with an intensification of L‐CAM, N‐CAM and general cadherin immunofluorescence in the forming clear‐Oberhautchen layers, and in the following beta‐ and alpha‐layers as they start to differentiate from the basal layer. A higher immunolabelling for cell adhesion cadherins suggests that these proteins contribute to form an integrated epidermal unit along the regenerating scales that allows the ordered stratification and shedding of these layers in lizard epidermis.

Climate Shapes the Geographic Distribution and Introgressive Spread of Color Ornamentation in Common Wall Lizards.

AbstractClimate can exert an effect on the strength of sexual selection, but empirical evidence is limited. Here, we tested whether climate predicts the geographic distribution and introgressive spread of sexually selected male color ornamentation across 114 populations of the common wall lizard, Podarcis muralis. Coloration was highly structured across the landscape and did not reflect genetic differentiation. Instead, color ornamentation was consistently exaggerated in hot and dry environments, suggesting that climate-driven selection maintains geographic variation in spite of gene flow. Introgression of color ornamentation into a distantly related lineage appears to be ongoing and was particularly pronounced in warm climates with wet winters and dry summers. Combined, these results suggest that sexual ornamentation is consistently favored in climates that allow a prolonged reproductive season and high and reliable opportunities for lizard activity. This pattern corroborates theoretical predictions that such climatic conditions reduce the temporal clustering of receptive females and increase male-male competition, resulting in strong sexual selection. In summary, we provide compelling evidence for the importance of climate for the evolution of color ornamentation, and we demonstrate that geographic variation in the strength of sexual selection influences introgression of this phenotype.

Moving to the city: testing the implications of morphological shifts on locomotor performance in introduced urban lizards

Abstract Understanding how morphology affects performance in novel environments and how populations shift their morphology in response to environmental selective pressures is necessary to understand how invaders can be successful. We tested these relationships in a global colonizer, the common wall lizard (Podarcis muralis), translocated to Cincinnati, OH, USA 70 years ago. We investigated how morphology shifts in this population inhabiting a novel environment, how these morphological shifts influence locomotor performance and how performance changes in novel conditions. We compared the morphology of museum specimens and current lizards to see which aspects of morphology have shifted over time. Although overall body size did not change, most body dimensions reduced in size. We measured sprint speed with a full-factorial design of substrate type, incline angle and obstacles. We identified a pattern of negative correlation in sprint performance between conditions with and without obstacles. The locomotor advantage of larger body size was diminished when obstacles were present. Finally, there was no relationship between individual variation in contemporary morphology and sprint performance, providing no support to the hypothesis that these shifts are attributable to selective pressures on locomotor performance in the conditions tested.

Do colour morphs of wall lizards express different personalities?

Abstract Colour morphs sometimes have different behavioural strategies which may be maintained by frequency or density dependence mechanisms. We investigated temporal changes in behavioural reaction to a novel environment among colour morphs (yellow, orange, white) of the European wall lizard (Podarcis muralis). Adult males were given two 15 min experimental trials, and their locomotion was highly consistent between the two trials. Boldness, freezing and escape behaviour were less repeatable. Colour morphs differed in their locomotion and freezing behaviour. Boldness was similar among the morphs, whereas escape behaviour was lowest in yellow morph. Consequently, yellow morph males tended to explore novel environments quickly and thus were more likely to move to potentially safe areas. Orange and white males showed more fear when exposed to a novel environment. Whether such alternative behavioural strategies can contribute to the maintenance of variable fitness optima among the morphs and ultimately to the maintenance of polymorphism remains open to further investigation.

Viability, behavior, and color expression in the offspring of matings between common wall lizard Podarcis muralis color morphs.

Color polymorphisms are widely studied to identify the mechanisms responsible for the origin and maintenance of phenotypic variability in nature. Two of the mechanisms of balancing selection currently thought to explain the long-term persistence of polymorphisms are the evolution of alternative phenotypic optima through correlational selection on suites of traits including color and heterosis. Both of these mechanisms can generate differences in offspring viability and fitness arising from different morph combinations. Here, we examined the effect of parental morph combination on fertilization success, embryonic viability, newborn quality, antipredator, and foraging behavior, as well as inter-annual survival by conducting controlled matings in a polymorphic lacertid Podarcis muralis, where color morphs are frequently assumed to reflect alternative phenotypic optima (e.g., alternative reproductive strategies). Juveniles were kept in outdoor tubs for a year in order to study inter-annual growth, survival, and morph inheritance. In agreement with a previous genome-wide association analysis, morph frequencies in the year-old juveniles matched the frequencies expected if orange and yellow expressions depended on recessive homozygosity at 2 separate loci. Our findings also agree with previous literature reporting higher reproductive output of heavy females and the higher overall viability of heavy newborn lizards, but we found no evidence for the existence of alternative breeding investment strategies in female morphs, or morph-combination effects on offspring viability and behavior. We conclude that inter-morph breeding remains entirely viable and genetic incompatibilities are of little significance for the maintenance of discrete color morphs in P. muralis from the Pyrenees.

Aggressive interactions between a sand lizard Lacerta agilis and a common wall lizard Podarcis muralis in England

Aggressive interactions between a sand lizard Lacerta agilis and a common wall lizard Podarcis muralis in England

Phenology and temperature are the main drivers shaping the detection probability of the common wall lizard

Abstract Measuring the abundance of organisms is essential to provide information to ecology and biodiversity conservation. Hardly ever, the probability of detecting an animal during a survey is near one. Overlooking this observational process can lead to biased estimates of population size and vital rates. In this study, through Bayesian modeling, I evaluated the effects of temperature, precipitation, wind, humidity, and phenology in determining changes in the detection probability of the common wall lizard, for which studies on the factors determining detection probability are currently not available. Additionally, I tested for two possible interactions: date-temperature and date-humidity, in order to assess if the relationships of these variables with detection probability vary through the sampling season. Detection probability was highest earlier in the season (April) and between 24 and 28 degrees. Rainfall during the survey showed a negative effect on detection probability. In contrast, cumulative precipitation in the 24 hours before the survey showed a positive relationship, indicating that lizards are easier to detect in surveys after rainy days. Furthermore, date and temperature showed a positive interaction, indicating that the relationship between detectability and temperature changed over the sampling season. Date and humidity showed a negative interaction: late in the sampling season, detectability was higher with lower humidity, however, this relationship was not found in the early season. Future studies can consider multiple sites to evaluate the extent of variation in the drivers of detection probability and to assess the factors related to abundance.

Close encounters of the three morphs: Does color affect aggression in a polymorphic lizard?

Color polymorphism is genetically controlled, and the process generating and maintaining morphs can affect speciation/extinction rates. Color badges are useful signals in intraspecific communication because they convey information about alternative strategies and can potentially decrease unnecessary conflicts among different color morphs. Competition and aggressive interactions among color morphs can contribute to polymorphism maintenance. This could lead to an uneven spatial distribution of morphs in a population because the local frequency of each morph establishes the intensity of the competition and the fitness of each male. We used a polymorphic lizard, Podarcis muralis, to assess if aggression varies among morphs under two contrasting hypotheses: a heteromorphic versushomomorphic aggression. We used laboratory mirror tests after lizard color manipulation, and we verified the consistency of results with an analysis of the spatial distribution of morphs in a wild population. Both the experiments confirmed that aggression is more common during homomorphic than heteromorphic contests. The adoption of alternative behavioral strategies that minimize risks and costs could facilitate the stable coexistence of the phenotypes and reduce competition. A bias in aggression would advantage rarer morph, which would suffer less harassment by common morphs obtaining a fitness advantage. This process would be negatively-frequency-dependent and would stabilize polymorphism, possibly contributing to sympatric speciation.

Climate and habitat configuration limit range expansion and patterns of dispersal in a non-native lizard.

Invasive species are one of the main causes of biodiversity loss worldwide. As introduced, populations increase in abundance and geographical range, so does the potential for negative impacts on native communities. As such, there is a need to better understand the processes driving range expansion as species become established in recipient landscapes. Through an investigation into capacity for population growth and range expansion of introduced populations of a non‐native lizard (Podarcis muralis), we aimed to demonstrate how multi‐scale factors influence spatial spread, population growth, and invasion potential in introduced species. We collated location records of P. muralis presence in England, UK through data collected from field surveys and a citizen science campaign. We used these data as input for presence‐background models to predict areas of climate suitability at a national‐scale (5 km resolution), and fine‐scale habitat suitability at the local scale (2 m resolution). We then integrated local models into an individual‐based modeling platform to simulate population dynamics and forecast range expansion for 10 populations in heterogeneous landscapes. National‐scale models indicated climate suitability has restricted the species to the southern parts of the UK, primarily by a latitudinal cline in overwintering conditions. Patterns of population growth and range expansion were related to differences in local landscape configuration and heterogeneity. Growth curves suggest populations could be in the early stages of exponential growth. However, annual rates of range expansion are predicted to be low (5–16 m). We conclude that extensive nationwide range expansion through secondary introduction is likely to be restricted by currently unsuitable climate beyond southern regions of the UK. However, exponential growth of local populations in habitats providing transport pathways is likely to increase opportunities for regional expansion. The broad habitat niche of P. muralis, coupled with configuration of habitat patches in the landscape, allows populations to increase locally with minimal dispersal.

Subjective resource value affects aggressive behavior independently of resource-holding-potential and color morphs in male common wall lizard

Game theory models predict the outcome of a dyadic contest to depend on opponents’ asymmetries in three main traits: resource-holding potential (RHP), resource value (RV) and aggressiveness. Using male common wall lizards Podarcis muralis, a polymorphic species showing three discrete morphs (white, yellow, and red), we investigated how the aggressive behavior varies according to a change in subjective RV and color morphs, while controlling for the asymmetry in RHP (using mirrors). By comparing the aggression of the same individual towards its mirror image in two different arenas (familiar = high subjective RV; novel = low subjective RV), we showed that lizard aggressive behavior was more intense and prolonged in the familiar arena than in the new one, thus supporting the occurrence of a direct relationship between motivation and aggression in this species. We also found the overall aggressiveness to differ from individual to individual, supporting the general hypothesis that aggressiveness is a trait associated with personality. By contrast, no effect of morphs was detected, ruling out the occurrence of morph specific variation in the aggressiveness. Our results highlight that an individual’s motivation and personality might be as important as RHP and RV in the resolution of animal contests.

Morph-specific seasonal variation of aggressive behaviour in a polymorphic lizard species.

The persistence of colour polymorphism (CP) within a given population is generally associated with the coexistence of alternative reproductive strategies, each one involving specific trade-offs among behavioural, morphological, physiological, and other life histories. Common wall lizard (Podarcis muralis), is a medium-sized diurnal lizard, showing CP in three main colours (yellow, white, and red) on throat and belly, and a morph-specific pattern for both immunocompetence and seasonal variation of T levels. Yellow males show low stamina with high plasma T levels at the beginning of the season, while white males show high stamina with a higher plasma T levels at the end of the season. We hypothesised the presence of two strategies: a risky one, characterised by high aggressiveness played by yellow-morph, and a conservative one by white morph with low aggressiveness. Thus, we tested the aggressive response to conspecifics of yellow and white morphs using a mirror inserted into their cage, mimicking an intrusion of a stranger in their territories, throughout the breeding season (from April to July, 117 trials). We considered three types of aggressive response, with different levels of aggressiveness: (i) bite against the image reflected in the mirror, (ii) seconds spent by the individuals into the half mirrored cage, and (iii) number of times the lizard entered the half mirrored cage. We also considered the number of tongue flicking as explorative behaviour variable. All lizards were tested after a period of acclimatisation to the captivity conditions. Results demonstrate that yellow males showed a higher aggressive response in the early season and a decrease aggressive response towards the end, whereas white males showed an opposite pattern.

No evidence for differential sociosexual behavior and space use in the color morphs of the European common wall lizard (Podarcis muralis).

Explaining the evolutionary origin and maintenance of color polymorphisms is a major challenge in evolutionary biology. Such polymorphisms are commonly thought to reflect the existence of alternative behavioral or life‐history strategies under negative frequency‐dependent selection. The European common wall lizard Podarcis muralis exhibits a striking ventral color polymorphism that has been intensely studied and is often assumed to reflect alternative reproductive strategies, similar to the iconic “rock–paper–scissors” system described in the North American lizard Uta stansburiana. However, available studies so far have ignored central aspects in the behavioral ecology of this species that are crucial to assess the existence of alternative reproductive strategies. Here, we try to fill this gap by studying the social behavior, space use, and reproductive performance of lizards showing different color morphs, both in a free‐ranging population from the eastern Pyrenees and in ten experimental mesocosm enclosures. In the natural population, we found no differences between morphs in site fidelity, space use, or male–female spatial overlap. Likewise, color morph was irrelevant to sociosexual behavior, space use, and reproductive success within experimental enclosures. Our results contradict the commonly held hypothesis that P. muralis morphs reflect alternative behavioral strategies, and suggest that we should instead turn our attention to alternative functional explanations.

Statistical methodology for the evaluation of leukocyte data in wild reptile populations: A case study with the common wall lizard (Podarcis muralis).

The leukocyte profile has the potential to be a reliable method to measure health conditions and stress in wild animals, but limitations occur because current knowledge on reference intervals is largely incomplete, especially because data come from studies on captive animals involving few individuals from single populations. Here we propose a general framework for achieving reliable leukocyte reference intervals, encompassing a set of internal and external factors, potentially affecting the leukogram. To do so, we present a systematic survey of the hematology of the common wall lizard, Podarcis muralis, involving 794 lizards from 54 populations over the whole geographic range of the species in Italy. Reference intervals for white blood cell (WBC) and leukocyte differential count were obtained by using linear mixed models in a Bayesian framework. The application of the procedure clearly showed that both internal (sex and size) and external (latitude and season) factors are a source of variation of leukocyte profile. Furthermore, the leukogram of common wall lizard has a strong variability among populations, which accounts for more than 50% of the whole variation. Consequently, some common assumptions used in studies on captive individuals are no longer supported in wild populations, namely, i) any group of individuals is a representative sample, ii) any population is representative of all others, iii) geographic clines do not occur over the species range, and iv) seasonal variation has limited effects. We encourage researchers aimed at the definition of leukocyte reference intervals for wild populations of reptiles to involve a large number of populations over a wide geographic range in ad hoc statistical models to disentangle local and geographic effects on leukocyte profile variation.

Response behaviour of native lizards and invading wall lizard to interspecific scent: implications for invasion success

The human-assisted movement of species beyond their native range facilitates novel interactions between invaders and native species that can determine whether an introduced species becomes invasive and the nature of any consequences for native communities. Avoiding costly interactions through recognition and avoidance can be compromised by the naivety of native species to novel invaders and vice versa. We tested this hypothesis using the common wall lizard, Podarcis muralis, and the native lizard species with which it may now interact in Britain (common lizard, Zootoca vivipara, sand lizard, Lacerta agilis) and on Vancouver Island (northern alligator lizard, Elgaria coerulea) by exploring species' responses (tongue flicks, avoidance behaviour) to heterospecific scent cues in controlled experiments. The tongue flick response of P. muralis depended on the different species’ scent, with significantly more tongue flicks directed to E. coerulea scent than the other species and the control. This recognition did not result in any other behavioural response in P. muralis (i.e. attraction, aggression, avoidance). Lacerta agilis showed a strong recognition response to P. muralis scent, with more tongue flicks occurring close to the treatment stimuli than the control and aggressive behaviour directed towards the scent source. Conversely, Z. vivipara spent less time near P. muralis scent cues than the control but its tongue flick rate was higher towards this scent in this reduced time, consistent with an avoidance response. There was no evidence of E. coerulea recognition of P. muralis scent in terms of tongue flicks or time spent near the stimuli, although the native species did show a preference for P. muralis-scented refuges. Our results suggest a variable response of native species to the scent of P. muralis, from an avoidance response by Z. vivipara that mirrors patterns of exclusion observed in the field to direct aggression observed in L. agilis and an ambiguous reaction from E. coerulea which may reflect a diminished response to a cue with a low associated cost. These results have significant implications for the invasive success and potential impacts of introduced P. muralis populations on native lizards.

Predation and ingestion of a viviparous lizard (Zootoca vivipara) by the common wall lizard (Podarcis muralis) in England

Predation and ingestion of a viviparous lizard (Zootoca vivipara) by the common wall lizard (Podarcis muralis) in England

The movement dynamics of autotomized lizards and their tails reveal functional costs of caudal autotomy.

Autotomy has evolved independently several times in different animal lineages. It frequently involves immediate functional costs, so regeneration evolved in many instances to restore the functionality of that body part. Caudal autotomy is a widespread antipredator strategy in lizards, although it may affect energy storage, locomotion dynamics, or survival in future encounters with predators. Here, we assessed the effect of tail loss on the locomotor performance of wall lizards (Podarcis muralis), as well as the recovery of locomotor functionality of lizards with regenerated tails, and the movement dynamics of shed tails that were either intact or having regenerated portions. Tail loss had no effect on locomotion over unhindered spaces, possibly due to compensation between a negative effect on the stride of front limbs, and a positive effect of losing mass and friction force. We found a clear negative impact of tail loss on locomotion in spaces with interspersed obstacles, in which tailed lizards jumped larger distances when leaving the obstacles. Besides, lizards that used the tail to push off the ground were able to approach the obstacles from further, so that the tail seemed to be useful when used during jumping. Regeneration fully restores lizard's locomotor capacities, but tail antipredator value, as indicated by the intensity of post-autotomic movements, is only partially retrieved. From these results, we propose that, together with the recovery of post-autotomy antipredator capacities, the restoration of the organismal locomotor performance may have been an important, yet frequently neglected factor in the evolution of lizard's regeneration ability.

Autoradiography and inmmunolabeling suggests that lizard blastema contains arginase-positive M2-like macrophages that may support tail regeneration

BackgroundThe regenerating blastema of the tail in the lizard Podarcis muralis contains numerous macrophages among the prevalent mesenchymal cells. Some macrophages are phagocytic but others are devoid of phagosomes suggesting that they have other roles aside phagocytosis. MethodsThe presence of healing macrophages (M2-like) has been tested using autoradiographic, immunohistochemical and ultrastructural studies. ResultsAutoradiography shows an uptake of tritiated arginine in sparse cells of the blastema and in the regenerating epidermis. Bioinformatics analysis suggests that epitopes for arginase-1 and -2, recognized by the employed antibody, are present in lizards. Immunofluorescence shows sparse arginase immunopositive macrophages in the blastema and few macrophages also in the apical wound epidermis. The ultrastructural study shows that macrophages contain dense secretory granules, most likely inactive lysosomes, and small cytoplasmic pale vesicles. Some of the small vesicles are arginase-positive while immunolabeling is very diffuse in the macrophage cytoplasm. ConclusionsThe presence of cells incorporating arginine and of arginase 1-positive cells suggests that M2-like macrophages are present among mesenchymal and epidermal cells of the regenerative tail blastema. M2-like macrophages may promote tail regeneration differently from the numerous pro-inflammatory macrophages previously detected in the scarring limb. The presence of M2-like macrophages in addition to hyaluronate, support the hypothesis that the regenerative blastema of the tail in lizards is an immuno-privileged organ where cell proliferation and growth occur without degenerating in a tumorigenic outgrowth.

The possible origin of the common wall lizard, Podarcis muralis (Laurenti, 1768) in Ukraine

The phylogenetic relationships and possible origin of a putative non-native population of Podarcis muralis in Ukraine were assessed based on sequences of the mitochondrial gene cytochrome b. Phylogenetic analysis showed that the Ukrainian lizards belong to two distinct mitochondrial lineages (haplogroups), both occurring within the Central Balkan clade, which includes most of central and south-eastern European populations. From overall three detected Ukrainian haplotypes, one haplotype share same genetic signal with the hyplotype from the locality Bjala (Bulgaria), the other two are unique for Ukrainian population. Two of haplotypes correspond with haplogroup covering large geographic region of Bulgaria, Serbia, and Romania. These results reinforce previous findings that the species has the ability to establish new populations out of its native range. While most introductions to Germany and Britain have been deliberate, it appears likely that human transport of goods via the Danube river of goods is responsible for the range expansion into Ukraine.

Biology and origin of isolated north-easternmost populations of the common wall lizard, Podarcis muralis

Abstract The common wall lizard, Podarcis muralis, is a widely distributed European lizard which has been often introduced across the continent, including north of the continuous species range. Three such populations were recently discovered in the Strzelin Hills in Poland, but no information is available about their origin. We studied the morphological variation, demographic structure and ecology of these populations, as well as their possible origin based on cytochrome b mtDNA sequences. Between 2011 and 2019, the lizards were annually active from the first half of March to mid-October. Males attained significantly larger snout-vent length than females and had relatively larger heads. Almost half of all captured individuals exhibited at least one pileus scale anomaly. Analysis of colour polymorphism revealed the occurrence of three morphs: white, white-red and red. The oldest lizards reached the age of 8 years. These parameters of Polish populations do not deviate from those of other populations from similar latitudes. Molecular analysis revealed that they belong to the most common haplotype of Central European haplogroup I of the Central Balkan clade. This haplotype is widely distributed across the Czech Republic and Slovakia; however, genetic data do not allow determination of the exact origin of the Polish population. Human-mediated introduction from the closest localities, the Czech Republic or Slovakia, is probable but the relict status cannot at present be excluded.