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Sexual selection and parasites of lizards

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Rodrigo Megía Palma
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Ontogeny is expected to be a determinant factor affecting production of colour patches in lizards, while immune challenges or sudden weight loss may impair the maintenance of pigment-based coloration within a breeding season. We translocated males of the lizard Psammodromus algirus between two sampling plots that differed in distance to a road, vegetation structure, and predator abundance. We analysed variation in spectral reflectance of their colour patches the same and the following year. The change in the reflectance of the lizard colour patches within the first breeding season was explained by the interaction between plot and treatment, but not body condition. The maintenance of the breeding coloration was impaired only in those males translocated close to the road, probably reflecting that it is a poor-quality habitat for P. algirus . The following year, lizards that produced a more elaborate coloration were those that increased their body condition and controlled some parasitic infections, although suffered an increase of others. This study shows that colour patch production is plastic in P. algirus . Lizards increasing parasites or losing weight reduced pigmentation, although habitat quality can cushion these negative effects on pigmentation. However, not all parasites constrain the investment in coloration. In fact, some increased in those lizards that allocated more pigments to colour patches. In conclusion, longitudinal studies following experimental manipulation can contribute to understand pigment allocation rules in lizards. Significance statement Pigments involved in colour patches of animals are limiting resources that can be reallocated off the skin to other functions. However, longitudinal evidence of this phenomenon is scarce in reptiles. We designed a manipulative mark-recapture experiment to investigate effects of habitat and parasitic infections on colour patch maintenance (within-year variation) and production (between-year variation) in male free-ranging lizards that were reciprocally translocated between two patches of habitat that differed in quality. During the first year, lizards translocated to the habitat with more predators and worse vegetation impoverished their coloration, while lizards translocated to the more favourable habitat maintained it despite all translocated lizards loose body condition. The next year we detected different effects on the coloration of three different parasites investigated, suggesting that coloration can reflect the virulence of the infections.
Rodrigo Megía Palma
added a research item
Several studies of lizards have made an erroneous interpretation of negative relationships between spectral brightness and parasite load, and thus provided misleading support for the Hamilton–Zuk hypothesis (HZH). The HZH predicts that infected hosts will produce poorer sexual ornamentation than uninfected individuals as a result of energetic trade-offs between immune and signalling functions. To test whether there is a negative relationship between spectral brightness and pigment content in the skin of lizards, we used spectrophotometry to quantify the changes in spectral brightness of colour patches of two species after chemically manipulating the contents of orange, yellow and black pigments in skin samples. Carotenoids were identified using high performance liquid chromatography. In addition, we compared the spectral brightness in the colour patches of live individuals with differential expression of nuptial coloration. Overall, the analyses demonstrated that the more pigmented the colour patch, the darker the spectrum. We provide a comprehensive interpretation of how variation in pigment content affects the spectral brightness of the colour patches of lizards. Furthermore, we review 18 studies of lizards presenting 24 intraspecific tests of the HZH and show that 14 (58%) of the tests do not support the hypothesis.
Rodrigo Megía Palma
added 2 research items
Parasites generally have a negative influence on the color expression of their hosts. Sexual selection theory predicts high quality resistant individuals should show intense coloration, whereas susceptible low quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infecting males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. These males were also more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria.
Rodrigo Megía Palma
added 3 research items
Communicative traits are strikingly diverse and may vary among populations of the same species. Within a population, these traits may also display seasonal variation. Chemical signals play a key role in the communication of many taxa. However, we still know far too little about chemical communication in some vertebrate groups. In lizards, only a few studies have examined interpopulational variation in the composition of chemical cues and signals and only one study has explored the seasonal effects. Here we sampled three subspecies of the Tenerife lizards ( Gallotia galloti ) and analyze the lipophilic fraction of their femoral gland secretions to characterize the potential interpopulational variation in the chemical signals. In addition, we assessed whether composition of these secretions differed between the reproductive and the non-reproductive season. We analyzed variations in both the overall chemical profile and the abundance of the two main compounds (cholesterol and vitamin E). Our results show interpopulational and seasonal differences in G. gallotia chemical profiles. These findings are in accordance with the high interpopulational variability of compounds observed in lizard chemical signals and show that their composition is not only shaped by selective factors linked to reproductive season.
Melanic pigments play a key role in the coloration of animals. However, the type of melanin pigment in black, brown, and blue colored scales of Squamata has not previously been studied. Based on research on birds and mammals we may expect that pheomelanin is the majority pigment in brownish colorations and eumelanin is the majority pigment in black and blue colorations of Squamata. In order to characterize the pigments that underlie the melanin-based colorations of lizards we have analyzed the skin of nine genera of lacertids using dispersive Raman spectroscopy. Our results suggest that no prediction can be made on the type of pigmentary melanin present in the skin of the lacertids based alone on the hue of the sample. Indeed, brownish patterns in the skin of Psammodromus, Gallotia, Acanthodactylus, and Algyroides lizards presented both chemical forms of melanin: eumelanin and pheomelanin. Thus, pheomelanogenesis might be an ancient characteristic within Lacertidae because it was detected in genera in the Lacertini, Eremini, and Gallotini. Raman spectra of melanic-based patterns of genus Zootoca and ultraviolet (UV)-blue patches of Podarcis, Iberolacerta, Lacerta, and Timon lizards suggested that eumelanin is the majority pigment in these patches. Raman spectroscopy is a suitable nondestructive technique useful to identify melanin forms in the skin of lizards and it demonstrated that pheomelanin is synthesized by Squamata.
Rodrigo Megía Palma
added 5 research items
During the mating season, male vertebrates may face a negative immunomodulation due to the increase of their plasma testosterone levels. These hormonal changes may lead to an increase in the susceptibility to parasitic diseases. During the mating season of 2013, 75 individuals of Lacerta scheriberi in a population breeding at middle elevation were screened for blood parasites, intestinal worms and ectoparasites. The prevalence and intensity of these three types of parasites in the individuals of the study population can be explained by the biology and type of transmission of these parasites and the sexual and behavioral ecology of the host lizard species. Adult male lizards living in humid bushes showed the highest levels of infection by ectoparasites. Even though there was no correlation between tick load and body condition, lizard where ticks were experimentally removed moved longer distances than those from the control group where ticks remain untouched. Moreover, the individuals with more ticks tended to have more intestinal worms. Furthermore, adult males infected by intestinal worms had a worse inflammatory skin reaction than those males without intestinal worms. Otherwise, adult male lizards with worse body condition moved less and had less parasite diversity. In relation with the hematic parasites, only adult individuals with better body condition were infected, suggesting a transmission of the parasite during intra and intersexual interactions. Therefore, these results agree with the idea that sex is costly in this population of the Iberian Schreiber's Green lizard, at least in terms of parasite infection.
Pigment-based ornaments in vertebrates may reflect the body condition or health status of the individual in correlation with environmental stress and hormonal balance. Among the environmental factors shaping sexual colouration, parasitic infections have been stressed as an important evolutionary pressure constraining the maintenance of pigment-based ornaments. However, the honesty of structure-based ornaments in vertebrates is still under debate. Structural UV-biased ornaments in Gallotia lizards were described as a trait used by conspecifics during mate and rival assessment suggesting the reliability of these signals. We investigated the relationship between parasitaemia, body condition and a structural-based ornament present in the cheek of the sexually dichromatic Canarian lacertid Gallotia galloti in a population with an almost 100 % prevalence of haemoparasites. Using spectrophotometric techniques, we found that males with higher values of cheek UV chroma were infected with more haemoparasites. No significant relationship was found between haemoparasite load and body condition. However, males with higher cheek UV chroma showed significantly better body condition. In addition, we found that cheek hue was significantly related to body condition of individuals in both sexes. In males, cheek reflectivity biased towards the UV range was significantly related to better body condition. In females, those individuals with better body condition showed more whitish cheeks with less UV suggesting that cheek hue serves as an intersexual signal for sex recognition. We conclude that the positive relationship between cheek chroma and parasite load in male lizards is compatible with both differential density of melanin and iridophore arrangement in the dermis conveying an individual’s ability to cope with environmental stress.
Host species in populations under strong pressures from parasitic diseases may evolve ornaments to signal individual host quality to conspecifics. Colour ornaments in lizards result from the interaction of different layers in the skin. When inner layers of melanin and well-arranged iridophores are combined, UV-blue structural colouration results. On the other hand, when layers of erythrophores are densely loaded with carotenoids, a UV-yellow colouration is seen. The expression of carotenoid-based traits has been frequently studied in relation to parasite infections. However, few studies have explored the relationship between parasitic diseases and structural colouration. In this study, we investigated the expression of UV-blue and UV-yellow throat colour patches in males of Lacerta schreiberi in relation to infection by haemoparasites, ixodid ticks and intestinal nematodes. The brightness of the UV-yellow throat patch (a carotenoid-based ornament) was positively correlated with body condition and negatively correlated with the number of attached ticks, supporting Hamilton and Zuk’s hypothesis. Additionally, individuals that passed nematode eggs in the faeces had UV-yellow throat patches with higher hue values (more greenish colouration). Strikingly, the individuals infected by haemoparasites of the genus Schellackia showed UV-blue throat patches (a melanin-based ornament) with higher values of both UV-blue chroma and hue (i.e., UV-biased throats) than did uninfected individuals, suggesting a key role for melanin in the nuptial colouration of this lizard species. Thus, the combined information from both UV-blue and UV-yellow throat patches may convey integrative information about individual quality in this lacertid species. Significance statement In this study, we present evidence that the striking throat colouration in males of the endemic Iberian green lizard is related to the presence or load of different parasites. The ornament is composed of one UV-yellow patch and one UV-blue patch, which were differentially related to the presence of different parasitic diseases in the individual hosts. These results suggest that different parasitic diseases may differentially constrain the expression of these colour patches. Moreover, the combined display of the two throat patches simultaneously may convey to conspecifics integrative information about the individual quality of the Iberian green lizard.