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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., Ventral color morphs in wall lizards have often been assumed to reflect alternative reproductive strategies. In this study, we study the social behavior, space use, and reproductive success of Podarcis muralis color morphs both in a free‐ranging population from the eastern Pyrenees and in ten experimental mesocosm enclosures. Overall, our results suggest that color morphs do not reflect alternative strategies concerning sociosexual behavior or space use.

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.

The Mediterranean Basin has experienced extensive change in geology and climate over the past six million years. Yet, the relative importance of key geological events for the distribution and genetic structure of the Mediterranean fauna remains poorly understood. Here, we use population genomic and phylogenomic analyses to establish the evolutionary history and genetic structure of common wall lizards (Podarcis muralis). This species is particularly informative because, in contrast to other Mediterranean lizards, it is widespread across the Iberian, Italian, and Balkan peninsulas, and in extra-Mediterranean regions. We found strong support for six major lineages within P. muralis, which were largely discordant with the phylogenetic relationship of mitochondrial DNA. The most recent common ancestor of extant P. muralis was likely distributed in the Italian Peninsula, and experienced an “Out-of-Italy” expansion following the Messinian salinity crisis (~5 Mya), resulting in the differentiation into the extant lineages on the Iberian, Italian and Balkan peninsulas. Introgression analysis revealed that both inter- and intraspecific gene flow have been pervasive throughout the evolutionary history of P. muralis. For example, the Southern Italy lineage has a hybrid origin, formed through admixture between the Central Italy lineage and an ancient lineage that was the sister to all other P. muralis. More recent genetic differentiation is associated with the onset of the Quaternary glaciations, which influenced population dynamics and genetic diversity of contemporary lineages. These results demonstrate the pervasive role of Mediterranean geology and climate for the evolutionary history and population genetic structure of extant species.

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.

Aposematic organisms can show phenotypic variability across their distributional ranges. The ecological advantages of this variability have been scarcely studied in vipers. We explored this issue in Vipera seoanei, a species that exhibits five geographically structured dorsal colour phenotypes across Northern Iberia: two zigzag patterned (Classic and Cantabrica), one dorsal-strip patterned (Bilineata), one even grey (Uniform), and one melanistic (Melanistic). We compared predation rates (raptors and mammals) on plasticine models resembling each colour phenotype in three localities. Visual modelling techniques were used to infer detectability (i.e. conspicuousness) of each model type for visually guided predators (i.e. diurnal raptors). We hypothesize that predation rates will be lower for the two zigzag models (aposematism hypothesis) and that models with higher detectability would show higher predation rates (detectability hypothesis). Classic and Bilineata models were the most conspicuous, while Cantabrica and Uniform were the less. Melanistic presented an intermediate conspicuousness. Predation rate was low (3.24% of models) although there was variation in attack frequency among models. Zigzag models were scarcely predated supporting the aposematic role of the zigzag pattern in European vipers to reduce predation (aposematism hypothesis). From the non-zigzag models, high predation occurred on Bilineata and Melanistic models, and low on Uniform models, partially supporting our detectability hypothesis. These results suggest particular evolutionary advantages for non-zigzag phenotypes such as better performance of Melanistic phenotypes in cold environments or better crypsis of Uniform phenotypes. Polymorphism in V. seoanei may respond to a complex number of forces acting differentially across an environmental gradient.

Divergence in sexually selected traits in allopatry should affect the degree and direction of hybridization. However, few studies have established the causes and targets of sexual selection during secondary contact. Common wall lizards (Podarcis muralis) from north-central Italy have highly exaggerated male sexual traits compared to populations in Western Europe. Using experimental populations, we show that this creates asymmetries in male dominance, spatial habitat use and reproductive success upon secondary contact. Hybridization occurred almost exclusively between males of the Italian lineage and females of the Western European lineage. We provide evidence to suggest stronger ongoing selection on male sexual traits within the dominant Italian lineage. However, these same characters did not predict hybridization, and hybrid matings contributed little to variance in male reproductive success. Instead, most hybrid offspring were sired by Italian males displaying phenotypes associated with lower within-lineage reproductive success. Thus, highly directional hybridization arises because some Italian males are out-competed within their own lineage but remain competitive relative to males of the other lineage. This pattern of hybridization is consistent with the direction of introgression in natural contact zones, but our data suggest that sexual selection acting through hybridization may be weak at the leading edge of natural hybrid zones. (Less)

Selection for signal efficacy (detectability) is an important factor driving the evolution of chromatic signals. Communication theory predicts that colour signals should evolve to show those properties that maximize their conspicuousness to receivers in their own visual environment. In the ventrally polymorphic lizard Podarcis muralis, visual modelling has shown morph-specific differences in chromatic conspicuousness (orange > yellow > white). Although this suggests that morphs may incur different detectability costs, the differences in conspicuousness could be compensated behaviourally if individuals of the more conspicuous morphs adopted postures that made their colour patches less visible. We quantified the degree of exposure of the lizard ventral and ventrolateral coloration in the field to investigate the relationship between body posture and colour morph. We used a classification based on four lizard postures, from ventral surface completely hidden to full exposure of the ventral and ventrolateral colour patches (when lizards extend their forelegs and raise the head). As these postures may have consequences for thermoregulation, we also recorded substrate and lizard body temperatures using a thermographic camera. Results did not reveal differences among morphs in the frequency with which they adopt postures that expose their colour patches. In contrast, we found a strong relationship between body temperature and lizard posture. Overall, our results support the view that, regardless of colour morph, perching wall lizards adopt the elevated postures that maximize exposure of their ventral colour patches only when their body temperature is high enough to allow for an efficient predator avoidance response. Selection for effective communication favours flashy, highly conspicuous coloration, but conspicuousness also makes colour signals more detectable to unintended receivers (e.g. predators). Some animals offset the costs associated with conspicuous coloration by evolving compensatory traits. In the lizard P. muralis, ventral colour morphs differ in conspicuousness and we hypothesized that the most conspicuous morphs might compensate for their increased conspicuousness by adopting postures that minimize exposure of their conspicuous colour patches. Results show that the morph-specific differences in conspicuousness are not compensated behaviourally. In contrast, we found a strong relationship between body temperature and lizard posture, suggesting that lizards, regardless of colour morph, adopt postures exposing their conspicuous colour patches only when their body temperature allows for an efficient predator avoidance response.

Iridescence is a visual property of those surfaces that change in colour with viewing angle. Iridescence has been rarely reported in reptiles, but some snakes and lizards show this type of coloration. Here we study the effect of different angles of light incidence and observation on the spectrophotometrically assessed reflectance of dorsal coloration in the lizard Podarcis muralis. The results demonstrate clear angle dependence of several colour parameters. In particular, different angles of light incidence and observation result in changes in hue of more than 30 nm. This suggests that lizard dorsal coloration may be perceived, depending on viewing geometry, as being of different colours by a wide range of potential observers. Functional implications of iridescence in dorsal coloration are discussed.

Colour polymorphisms are thought to be maintained by complex evolutionary processes some of which require that the colours of the alternative morphs function as chromatic signals to conspecifics. Unfortunately, a key aspect of this hypothesis has rarely been studied: whether the study species perceives its own colour variation as discrete rather than continuous. The European common wall lizard (Podarcis muralis) presents a striking colour polymorphism: the ventral surface of adults of both sexes may be coloured orange, white, yellow, or with a mosaic of scales combining two colours (orange-white, orange-yellow). Here we use a discrimination learning paradigm to test if P. muralis is capable of discriminating colour stimuli designed to match the ventral colours of conspecifics. We trained 20 lizards to eat from colour-coded wells bored in wooden blocks. Blocks had four colour-coded wells (orange, white, yellow, and an achromatic control), but only one contained food (mealworm larvae). After six trials, the lizards performed significantly better than expected by chance, showing a decrease in both the number of wells explored and the latency to finding the food. Using visual modelling techniques we found that, based on their spectral properties and the lizards’ cone sensitivities, the ventral colours of P. muralis correspond to discrete rather than continuous colour categories, and that colour discriminability (i.e. distance in perceptual space) varies depending on the morphs compared, which may have implications for signal detection and discrimination. These results suggest that P. muralis can discriminate hue differences matching their own ventral colour variation.

Chromatic signals result from the differential absorption of light by chemical compounds (pigment-based colours) and/or from differential scattering of light by integument nanostructures (structural colours). Both structural and pigment-based colours can be costly to produce, maintain and display, and have been shown to convey information about a variety of individual quality traits. Male wall lizards, Podarcis muralis, display conspicuously coloured ventral and lateral patches during ritualized inter- and intrasexual displays: ventral colours (perceived as orange, yellow or white by humans) are pigment based, while the ultraviolet (UV)-blue of the outer ventral scales (OVS), located along the flanks, is structurally produced. We used spectrophotometric data from 372 adult males to examine, considering the entire visual spectrum of lizards, whether ventral and OVS colour variables can predict male quality. Results indicate that the hue and UV chroma of OVS are good predictors of fighting ability (size-independent bite force) and body condition, respectively. This suggests that structural colour patches are condition dependent and function as complex multicomponent signals in this species. In contrast, ventral coloration apparently does not function as a male quality indicator. We suggest that ventral and lateral colour patches may be social signals with different information content, possibly aimed at different receivers.

Sexual selection is one of the main processes involved in the emergence and maintenance of heritable colour polymorphisms in a variety of taxa. Here we test whether the intensity of sexual selection, estimated from population sex ratio, predicts morph diversity in Podarcis muralis, a colour polymorphic lizard with discrete white, yellow, orange, white-orange, and yellow-orange male and female phenotypes (i.e. morphs). In a sample of 116 Pyrenean populations and 5421 lizards, sex ratios (m/f) vary from 0.29 to 2.5, with the number of morphs for each sex ranging from 2 to 5. Male-biased sex ratios are associated with increased morph diversity as measured with Shannon's diversity index. The main factor accounting for this relationship is male morph richness (i.e. the number of morphs). In contrast, female morph diversity is not related to sex ratio. These results suggest a relationship between the intensity of male intrasexual competition and male morph diversity. While other selective forces may interact with sexual selection in maintaining the colour polymorphisms in P. muralis, this evidence suggests a complex evolutionary scenario possibly involving frequency-dependent selection of alternative reproductive tactics and/or complex balancing selection. This article is protected by copyright. All rights reserved

Previous work with a colour polymorphic population of Podarcis muralis (Lacertidae) revealed that lizards pair by ventral colour, favouring the same colour (i.e. homomorphic) pairs. Such assortative pairing, which probably results in colour assortative mating, can have consequences for the genetic structure of the population and potentially promote speciation. The population previously studied, located in the Pyrenees, encompasses white, yellow and orange animals, as well as intermediate white-orange and yellow-orange morphs. However, other Pyrenean populations of P. muralis have less ventral colour morphs. Our aim in this study is to test the generality of the assortative colour pairing system, extending our previous analyses to populations with different morph compositions and frequencies. The results show that the assortative pattern of pairing is similar in all the populations analysed and, hence, independent of morph composition and not restricted to pentamorphic populations. This suggests that assortative pairing by colour is a general phenomenon for colour polymorphic populations of P. muralis.

Color polymorphisms are common in lizards, which provide an excellent model system to study their evolution and adaptive function. The lacertid genus Podarcis is particularly interesting because it comprises several polymorphic species. Previous studies with lacertid lizards have tried to explain the maintenance of color polymorphisms by correlational selection between color morphs and several phenotypic traits. Particular attention has been paid to their putative role as signals reflecting alternative reproductive strategies under frequency-dependent selection, but the relationship between mating patterns and color polymorphism has not been previously considered. In this study, we use longitudinal behavioral data obtained during six consecutive breeding seasons (2006-2011) in a free-ranging polymorphic population of Podarcis muralis lizards to examine the hypothesis that lizards mate assortatively by color. We provide spectrophotometric data that confirm the existence of discrete color morphs and show that morphs are ontogenetically stable once they develop fully in sexually mature individuals. We also present data on the year-to-year variation of relative morph frequencies. Finally, we provide evidence that, over a 6-year period, homomorphic male-female pairs in the wild were significantly more common than heteromorphic pairs. Taken together, our results suggest that color assortative mating may be involved in the maintenance of discrete color morphs in this and other lacertid species. © 2012 The Author.

Ultraviolet (UV) colorations have garnered extensive theoretical and empirical treatment in recent years, although the majority of studies have concerned themselves with avian taxa. However, many lizards have acute visual systems with retinal photoreceptors that are sensitive to UV wavelengths, and also display UV-reflecting colour patches. In the present study, we used UV photography and full-spectrum reflectance spectrophotometry to describe intra- and intersexual colour variation in adult ocellated lizards Lacerta (Timon) lepida and to obtain evidence of UV-based ornamentation. We also investigated whether any colour traits correlate with morphological traits potentially related to individual quality. The results obtained show that the prominent eyespots and blue outer ventral scales (OVS) that ocellated lizards have on their flanks reflect strongly in the UV range and are best described as UV/blue in coloration. The eyespots of males are larger and cover a larger surface area than those of females. However, these differences can be entirely accounted for by sex differences in body size, with males being generally larger than females. We also found differences in the shape of reflectance curves from males and females, with the eyespots and blue OVS of males being more UV-shifted than those of females. Other body regions have extremely low UV reflectance and are not sexually dichromatic. Eyespot size and the total surface area covered by eyespots increases with body size in males but not in females, suggesting that they may be signalling an intrinsic individual characteristic such as body size or male fighting ability. We also discuss the alternative and non-exclusive hypothesis that eyespots may function in lizards of both sexes as protective markings against predators. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 766–780.

Hybridisation is increasingly recognised as an important cause of diversification and adaptation. Here, we show how divergence in male secondary sexual characters between two lineages of the common wall lizard (Podarcis muralis) gives rise to strong asymmetries in male competitive ability and mating success, resulting in asymmetric hybridisation upon secondary contact. Combined with no negative effects of hybridisation on survival or reproductive characters in F1-hybrids, these results suggest that introgression should be asymmetric, resulting in the displacement of sexual characters of the sub-dominant lineage. This prediction was confirmed in two types of secondary contact, across a natural contact zone and in two introduced populations. Our study illustrates how divergence in sexually selected traits via male competition can determine the direction and extent of introgression, contributing to geographic patterns of genetic and phenotypic diversity.

Ultraviolet (UV) vision and UV colour patches have been reported in a wide range of taxa and are increasingly appreciated as an integral part of vertebrate visual perception and communication systems. Previous studies with Lacertidae, a lizard family with diverse and complex coloration, have revealed the existence of UV-reflecting patches that may function as social signals. However, confirmation of the signalling role of UV coloration requires demonstrating that the lizards are capable of vision in the UV waveband. Here we use a multidisciplinary approach to characterize the visual sensitivity of a diverse sample of lacertid species. Spectral transmission measurements of the ocular media show that wavelengths down to 300 nm are transmitted in all the species sampled. Four retinal oil droplet types can be identified in the lacertid retina. Two types are pigmented and two are colourless. Fluorescence microscopy reveals that a type of colourless droplet is UV-transmitting and may thus be associated with UV-sensitive cones. DNA sequencing shows that lacertids have a functional SWS1 opsin, very similar at 13 critical sites to that in the presumed ancestral vertebrate (which was UV-sensitive) and other UV-sensitive lizards. Finally, males of Podarcis muralis are capable of discriminating between two views of the same stimulus that differ only in the presence/absence of UV radiance. Taken together, these results provide convergent evidence of UV vision in lacertids, very likely by means of an independent photopigment. Moreover, the presence of four oil droplet types suggests that lacertids have a four-cone colour vision system.

Under certain circumstances, prey may inform potential predators of their unprofitability by means of pursuit-deterrent signals. The evidence for pursuit-deterrent signaling in reptiles is scant and taxonomically biased. Wall lizards, Podarcis muralis (Squamata: Lacertidae) produce several distinct types of stereotyped foot shake displays, of which one, performed in antipredator contexts, is a likely candidate for a pursuit-deterrent function. We investigated this possibility by recording the responses of lizards in the field to a slowly approaching human acting as a surrogate predator. In addition to starting and flight initiation distances, we measured the presence of foot shakes, the leg that was shaken, and the distance from the observer at which the display was performed (display distance). Of a total of 484 approaches, 109 (22.5%) elicited foot shake displays. Roughly half the lizards displayed from the location where they were first sighted, while the other half moved a short distance, then displayed. There was no left-right preference in the leg used to display, but most lizards displayed with the leg closer to the approaching predator. Juveniles and subadults had smaller flight initiation distances than adult lizards. There were no sex-related differences in starting or flight initiation distances, but females, for a given distance, were more likely to display than males. Foot shake display frequency declined abruptly at 1 m. If lizards waited until the surrogate predator was this close, they mostly fled without displaying. Our results show that antipredator foot shaking in P. muralis is consistent with expectations from pursuit-deterrent theory.