Sexual selection drives asymmetric introgression in wall lizards.

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 natur…

Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard

Significance Reptiles show an amazing color diversity based on variation in melanins, carotenoids, and pterins. This study reveals genes controlling differences between three color morphs (white, orange, and yellow) in the common wall lizard. Orange pigmentation, due to high levels of orange/red pterins in skin, is caused by genetic changes in the sepiapterin reductase gene. Yellow skin, showing high levels of yellow carotenoids, is controlled by the beta-carotene oxygenase 2 locus. Thus, the color polymorphism in the common wall lizard is associated with changes in two small regions of the genome containing genes with crucial roles in pterin and carotenoid metabolism. These genes are likel…

Differences in conspicuousness between alternative color morphs in a polychromatic lizard

In polychromatic species, differences in conspicuousness among alternative color morphs may affect the costs and benefits relating to signal detectability by primary receivers and unintended observers. Using visual modeling, we studied the conspicuousness of the body coloration in a ventrally polychromatic population of common wall lizards (Podarcis muralis). This species shows a complex color pattern that combines brown dorsal coloration, long-wavelength–biased ventral coloration, and ventrolateral ultraviolet (UV)-blue patches that are used to signal male quality. Considering simultaneously the visual system of P. muralis and lizard predators, we quantified the chromatic and achromatic (i…

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…

"Predator-elicited foot shakes in wall lizards (Podarcis muralis): Evidence for a pursuit-deterrent function": Correction to Font, Carazo, Pérez i de Lanuza, and Kramer (2012).

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

Abstract 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 we…

Visió en color i coloracions dels lacèrtids

Encara que els llangardaixos de la família Lacertidae mostren unes coloracions ornamentals molt cridaneres i variables, els estudis recents han tendit a menystenir la seua funció potencial per a la comunicació. El primer objectiu d’aquesta tesi ha estat l’estudi de la percepció del color per part dels lacèrtids, incloent la possibilitat que puguen ser capaços de percebre la porció ultraviolada pròxima (UVA) de l’espectre electromagnètic. Basant-nos en la informació obtinguda al respecte, he realitzat un estudi en profunditat del patró de coloració dels lacèrtids, la seua evolució i el seu paper en la cripsi i la comunicació. Els resultats obtinguts indiquen que els lacèrtids tenen una visió…

Experimental contact zones reveal causes and targets of sexual selection in hybridizing lizards

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 sel…

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 …

Regulatory Changes in Pterin and Carotenoid Genes Underlie Balanced Color Polymorphisms in the Wall Lizard

ABSTRACTReptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard, which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions, near genes associated with pterin (SPR) and carotenoid metabolism (BCO2), demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been co-opted for bright coloration in reptiles and indi…

Population genomics of wall lizards reflects the dynamic history of the Mediterranean Basin

AbstractThe 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, w…

Color-assortative mating in a color-polymorphic lacertid lizard

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 long…

Intensity of male-male competition predicts morph diversity in a color polymorphic lizard.

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 ma…

Colour patch size and measurement error using reflectance spectrophotometry

1 - Over the past twenty years, portable and relatively affordable spectrophotometers have greatly advanced the study of animal coloration. However, the small size of many colour patches poses methodological challenges that have not, to date, been assessed in the literature. Here, we tackle this issue for a reflectance spectrophotometry set-up widely used in ecology and evolution (the beam method). 2 - We reviewed the literature on animal coloration reporting the use of reflectance spectrophotometry to explore how the minimum measurable size of a colour patch is determined. We then used coloured plastic sheets to create artificial colour patches, and quantify the relationship between colour…

Iridescent (angle-dependent reflectance) properties of dorsal coloration in Podarcis muralis (Laurenti, 1768)

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…

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

Abstract 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 spec…

Through the eye of a lizard: hue discrimination in a lizard with ventral polymorphic coloration.

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…

Colours of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard

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 …

Ultraviolet vision in lacertid lizards: evidence from retinal structure, eye transmittance, SWS1 visual pigment genes, and behaviour

Abstract 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 ocula…

Ultraviolet reflectance and cryptic sexual dichromatism in the ocellated lizard, Lacerta (Timon) lepida (Squamata: Lacertidae)

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 indiv…

Ultraviolet reflectance of male nuptial colouration in sand lizards (Lacerta agilis) from the Pyrenees

Abstract The evolutionary significance of lacertid colourations is relatively unexplored. However, several studies have demonstrated signalling by means of bright green colouration in Swedish Lacerta agilis males during the breeding season. Unfortunately, most of these studies have been based on human colour perception that differs in several ways from that of lizard. An important difference between human and lizard colour vision is the presence of an ultraviolet (UV) sensitive cone in lizards. The available evidence suggests that male sand lizards colorations do not reflect UV wavelengths, at least in Swedish populations. However, this study, based on objective (spectrophotometric) measur…

Data from: The evolution of colour pattern complexity: selection for conspicuousness favours contrasting within-body colour combinations in lizards

Many animals display complex colour patterns that comprise several adjacent, often contrasting colour patches. Combining patches of complementary colours increases the overall conspicuousness of the complex pattern, enhancing signal detection. Therefore, selection for conspicuousness may act not only on the design of single colour patches, but also on their combination. Contrasting long- and short-wavelength colour patches are located on the ventral and lateral surfaces of many lacertid lizards. As the combination of long- and short-wavelength-based colours generates local chromatic contrast, we hypothesized that selection may favour the co-occurrence of lateral and ventral contrasting patc…

Data from: Experimental contact zones reveal causes and targets of sexual selection in hybridizing lizards

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 sel…

Data from: Colour patch size and measurement error using reflectance spectrometry

1. Over the past twenty years, portable and relatively affordable spectrophotometers have greatly advanced the study of animal coloration. However, the small size of many colour patches poses methodological challenges that have not, to date, been assessed in the literature. Here, we tackle this issue for a reflectance spectrophotometry set-up widely used in ecology and evolution (the beam method). 2. We reviewed the literature on animal coloration reporting the use of reflectance spectrophotometry to explore how the minimum measurable size of a colour patch is determined. We then used coloured plastic sheets to create artificial colour patches, and quantify the relationship between colour p…