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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.
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... For these species, colour patch expression is expected to be cheaper compared to carotenoid-based patches (Johnson and Fuller 2015). Nonetheless, a combination of these three pigment families usually produces colour patches in lizards rather than separate pigments alone (Andrade et al. 2019;Megía-Palma et al. 2021). ...
... Pterins are pigments present in yellow, orange, and red colour patches of lizards (Weiss et al. 2012;Cuervo et al. 2016;Andrade et al. 2019;Megía-Palma et al. 2021), while melanins participate in black, brown, and blue patches (Megía-Palma et al. 2018a). Recent investigations suggest that pterins and melanins are also reallocated off colour patches when lizards are immunologically challenged Megía-Palma et al. 2018b). ...
... Under this circumstance, some parasites may benefit from host's trade-offs in resource allocation and increase their intensity of infection in individuals allocating more resources to reproduction (Nordling et al. 1998;Knowles et al. 2009). Indeed, this latter hypothesis might explain why 58% of the published relationships between colour patch expression and parasite infection in lizards contradict the parasite-mediated selection hypothesis (see Megía-Palma et al. 2021). ...
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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.
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Individual variation in parasite exposure is often overlooked in studies of the role of parasites in the evolution of mate choice. Here we outline how androgen and carotenoid dependent red breeding coloration might broadcast reliable information about parasite exposure and genetic resistance to common parasites in a population of male three-spined sticklebacks (Gasterosteus aculeatus). Copepods, which are important prey for sticklebacks contain carotenoids essential for development of breeding coloration, but are also intermediate hosts for common parasites of sticklebacks. Of the five parasite species found in 46 males, only those three transmitted through copepods show associations with intensity of red breeding coloration. Two of these (Diphyllobothrium spp.) show a positive relationship with intensity of red coloration, whereas the apparently more pathogenic Schistocephalus solidus is negatively associated with intensity of red breeding coloration. The signal broadcasted by bright red males may thus be operating both as a sexually selected handicap, and as a reliable signal about degree of parasite exposure.
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Cnemidophorus arubensis, an endemic teiid lizard of Aruba island, Netherlands Antilles, is parasitized by a haemogregarine protozoan. The proportion of animals infected (prevalence) was greater for males than females and for adults compared to juveniles. Brightly colored males were more likely to be infected than blandly colored males of the same body size. Percent of erythrocytes infected with parasite gametocytes, and parasite prevalence, were similar in both wet and dry seasons. Infected and noninfected lizards were similar for several hematological, physiological, anatomical, and behavioral measures of parasite virulence. The Aruban haemogregarine appears to have an avirulent effect on Cnemidophorus arubensis.
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In spiny-footed lizards (Acanthodactylus erythrurus), adult females (but not males) show conspicuous red colouration in the tail and hind legs. To investigate the function of this red colouring and proximal causes of seasonal colour change, we captured adult females before the reproductive season and kept them in captivity in one of the three following situations: with a male and fertilization possible, with a male and fertilization impossible, or with another female (fertilization also impossible). Colour was quantified using spectrophotometry. Red colouration increased shortly before the onset of reproduction, but faded during the breeding season and became whitish (light buff-gray) in all cases. Both fertilized and unfertilized females laid eggs or were gravid after two months of the experiment, but while fertilized females laid mostly fertile eggs, unfertilized females only laid infertile eggs. Both egg formation and colour change might be triggered by abiotic factors, although female characteristics also play a role, since heavier females changed colour and laid eggs earlier. Females interacting freely with a male were darker at the end of the breeding season than females separated from the male, indicating that fertilization or physical contact might also have an effect on colouration. Colour change patterns found in this study suggest that female red colouration might have a mating-related function, but do not support a courtship rejection function for the red colour. However, whitish colouration resulting from red fading might signal gravidity in this species. Future experimental manipulation of female colouration will be needed to test these hypotheses.
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The selective forces imposed by primary receivers and unintended eavesdroppers of animal signals often act in opposite directions, constraining the development of conspicuous coloration. Because iridescent colours change their chromatic properties with viewer angle, iridescence offers a potential mechanism to relax this trade-off when the relevant observers involved in the evolution of signal design adopt different viewer geometries. We used reflectance spectrophotometry and visual modelling to test if the striking blue head coloration of males of the lizard Lacerta schreibeiri (1) is iridescent and (2) is more conspicuous when viewed from the perspective of conspecifics than from that of the main predators of adult L. schreibeiri (raptors). We demonstrate that the blue heads of L. schreiberi show angle-dependent changes in their chromatic properties. This variation allows the blue heads to be relatively conspicuous to conspecific viewers located in the same horizontal plane as the sender, while simultaneously being relatively cryptic to birds that see it from above. This study is the first to suggest the use of angle-dependent chromatic signals in lizards, and provides the first evidence of the adaptive function of iridescent coloration based on its detectability to different observers.
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Hamilton and Zuk proposed a good-genes model of sexual selection in which genetic variation can be maintained when females prefer ornaments that indicate resistance to parasites. When trait expression depends on a male's resistance, the co-adaptive cycles between host resistance and parasite virulence provide a mechanism in which genetic variation for fitness is continually renewed. The model made predictions at both the intraspecific and interspecific levels. In the three decades since its publication, these predictions have been theoretically examined in models of varying complexity, and empirically tested across many vertebrate and invertebrate taxa. Despite such prolonged interest, however, it has turned out to be extremely difficult to empirically demonstrate the process described, in part because we have not been able to test the underlying mechanisms that would unequivocally identify how parasites act as mediators of sexual selection. Here, we discuss how the use of high-throughput sequencing datasets available from modern genomic approaches might improve our ability to test this model. We expect that important contributions will come through the ability to identify and quantify the suite of parasites likely to influence the evolution of hosts' resistance, to confidently reconstruct phylogenies of both host and parasite taxa, and, perhaps most exciting, to detect generational cycles of heritable variants in populations of hosts and parasites. Integrative approaches, building on systems undergoing parasite-mediated selection with genomic resources already available, will be particularly useful in moving toward robust tests of this hypothesis. We finish by presenting case studies of well-studied host-parasite relationships that represent promising avenues for future research.
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The handicap hypothesis broadly argues that ornamental traits and displays are costly to produce and are a function of individual quality and condition. Consequently, the extent of ornament expression can act as an honest indicator of quality, condition or susceptibility to parasites, and influence the behavior of mates or competitors. We used reflectance spectrometry to quantify non-iridescent, ultraviolet (UV) and blue structurally-based plumage color and character size in relation to individual condition (feather growth rate) and occurrence of disease caused by a parasite infestation (knemidokoptic mange) in wild male Steller’s jays (Cyanocitta stelleri). We then attempted to experimentally reduce parasite load prior to molt and quantified the relative change in plumage and condition. Those birds with faster feather growth rates (i.e., in better condition) had lower hues (i.e., reflected shorter wavelengths, displaying a more intense, brilliant UV-blue color), suggesting the possibility of condition or feather growth rate-dependent production of color. We found that UV reflectance (UV chroma) was positively related to the occurrence of disease. We detected no effect of experimental treatment on plumage or condition. In conclusion, our results are suggestive of possible condition-dependent development of structurally-based plumage, and the positive relationship between macro-parasite– caused disease intensity and UV blue plumage color, demonstrated for the first time in this study, did not support the parasite-mediated handicap hypothesis.
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Colour traits in animals play critical roles in thermoregulation, photoprotection, camouflage, and visual communication and are amenable to objective quantification and modelling. However, the extensive variation in non-melanic pigments and structural colours in squamate reptiles has been largely disregarded. Here, we use an integrated approach to investigate the morphological basis and physical mechanisms generating variation in colour traits in tropical day geckos of the genus Phelsuma. Combining histology, optics, mass spectrometry, as well as UV and Raman spectroscopy, we show that the extensive variation in colour patterns observed within and among Phelsuma species is generated by complex interactions between, on the one hand, chromatophores containing yellow/red pteridine pigments and, on the other hand, iridophores producing structural colour by constructive interference of light with guanine nanocrystals. More specifically, we show that (i) the hue of the vivid dorso-lateral skin is modulated both by variation in geometry of structural highly-ordered narrowband reflectors and by the presence of yellow pigments, and (ii) the reflectivity of the white belly, as well as of dorso-lateral pigmentary red marks, is increased by underlying structural disorganised broadband reflectors. Most importantly, these interactions require precise co-localisation of yellow and red chromatophores with different types of iridophores, characterised by ordered and disordered nanocrystals, respectively. We validated these results through numerical simulations combining pigmentary components with a multilayer interferential optical model. Finally, we show that melanophores form dark lateral patterns but do not significantly contribute to variation in blue/green or red coloration, and that changes in the pH- or redox-state of pigments provide yet an additional source of colour variation in squamates. Precisely co-localised interacting pigmentary and structural elements generate extensive variation in lizard colour patterns. Our results indicate the need to identify the developmental mechanisms responsible for the control of nanocrystals size, shape and orientation, as well as the superposition of specific chromatophore types. This study opens up new perspectives for Phelsuma lizards as models in evolutionary developmental biology.
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Parasites influence colorful ornaments and their behavioral display in many animal hosts. Because coloration and display behavior are often critical components of communication, variation in these traits may have important implications for individual fitness, yet it remains unclear whether such traits are signals of quality in many taxa. We investigated the association between ectoparasitic mite load and the color and behavioral use of the throat fan (dewlap) by male Anolis brevirostris lizards. We found that heavily parasitized lizards exhibited lower body condition, duller dewlaps, and less frequent dewlap displays than less parasitized individuals. Our results thus suggest that highly parasitized individuals invest less in both ornamental color and behavioral display of that color. Because the two components of the signal simultaneously provide information on male quality, this study provides novel support for the long-standing hypothesis that colorful traits may function as social or sexual signals in reptiles.
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Parasites affect the life-histories and fitness of their hosts. It has been demonstrated that the ability of the immune system to cope with parasites partly depends on environmental conditions. In particular, stressful conditions have an immunosuppressive effect and may affect disease resistance. The relationship between environmental stress and parasitism was investigated using a blood parasite of the common lizard Lacerta vivipara. In laboratory cages, density and additional stressors had a significant effect on the intensity of both natural parasitaemia and parasitaemia induced by experimental infection. Four weeks after infection, crowded lizards had three times more parasites than noncrowded lizards. After 1 month of stress treatment, naturally infected lizards had a significantly higher level of plasma corticosterone and a higher parasite load than nonstressed individuals. In seminatural enclosures, stress induced by the habitat quality affected both the natural blood parasite prevalence and the intensity of parasitaemia of the host.
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I studied the activity, spacing patterns, courtship behavior, and survival of males (classified into two groups according to the development of the sexual coloration of the head) and females from a population of the lacertid lizard Psammodromus algirus. Brightly colored (C +) males were significantly larger (and probably older) than dull-colored (C −) males, but aspects of behavior differed between study years. In 1989, C+ males had larger home ranges, were more active, overlapped with more females, and courted females more frequently than C− males. In 1990, none of these traits differed between the two categories of males. The variables associated with survival were different in the two sexes. Larger and more active males survived less well than smaller and less active ones, whereas survival of females was related to the fact that the times when they were observed were later in the day. Higher mortality rates could have been due to a higher predation risk affecting animals that were active on more days or under less favorable conditions. I postulate that the increased activity of males (mainly category C+ in years favoring stronger selection) would increase their short-term reproductive success but negatively affect their survival.
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During female mate choice, conspicuous male sexual signals are used to infer male quality and choose the best sire for the offspring. The theory of parasite-mediated sexual selection (Hamilton-Zuk hypothesis) presumes that parasite infection can influence the elaboration of sexual signals: resistant individuals can invest more energy into signal expression and thus advertise their individual quality through signal intensity. By preferring these males, females can provide resistance genes for their offspring. Previous research showed that nuptial throat colour of male European green lizard, Lacerta viridis, plays a role in both inter- and intrasexual selections as a condition-dependent multiple signalling system. The aim of this study was to test the predictions of the Hamilton-Zuk hypothesis on male European green lizards. By blood sampling 30 adult males during the reproductive season, we found members of the Haemogregarinidae family in all but one individual (prevalence = 96 %). The infection intensity showed strong negative correlation with the throat and belly colour brightness in line with the predictions of the Hamilton-Zuk hypothesis. In addition, we found other correlations between infection intensity and other fitness-related traits, suggesting that parasite load has a remarkable effect on individual fitness. This study shows that throat patch colour of the European green lizards not only is a multiple signalling system but also possibly acts as an honest sexual signal of health state in accordance with the Hamilton-Zuk hypothesis.
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Color is used in social signaling by many species. Male Eastern Fence Lizards, Sceloporus undulatus, possess sex-specific dorsal and ventral coloration, including vivid blue badges on their throat and abdomen, which they behaviorally display to conspecifics. The presence of abdominal badges serves as a signal of an individual’s sex, but the significance of badge and integument coloration for signaling fitness traits is unknown. We tested for associations between coloration (color of the dorsal surface, chest, and abdominal and throat badges, as well as relative badge size) and a range of fitness-relevant morphological traits (body size and condition, tail and hind-limb length, and head size) in male Eastern Fence Lizards from two sites. Larger males have darker colored abdominal badges and relatively larger abdominal and throat badges. Males with longer tails and wider heads have darker dorsal coloration, and there is a correlation between head length and the color of the black abdominal badges, but this is not consistent between sites. Adults also have darker chest and dorsal coloration than do juveniles. These relationships suggest that S. undulatus color may signal competitive ability to male opponents. However, if this were the case, we would expect body condition and limb length, morphological measures that are tightly correlated with these fitness traits, to also correlate with coloration. This was not evident from our data. Therefore, despite significant variation in coloration of male S. undulatus, it is unlikely to reflect fitness associated with the traits measured in this study.
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Repeatability is a useful tool for the population geneticist or genetical ecolo- gist, but several papers have carried errors in its calculation. We outline the correct calcu- lation of repeatability, point out the common mistake, show how the incorrectly calculated value relates to repeatability, and provide a method for checking published values and calculating approximate repeatability values from the F ratio (mean squares among groups/ mean squares within groups).
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According to the hypothesis of parasite-mediated sexual selection, for a communication system to work reliably, parasites should reduce the showiness of sexual signals of their host. In this study, we examined whether the expression of breeding coloration in free-ranging adult European Green Lizards (Lacerta viridis (Laurenti, 1768)) is linked with infestation by their common ectoparasite Ixodes ricinus (L., 1758) (Acari: Ixodidae). We found that tick infestation was higher in males than in females. Males showing relatively heavier body for their tail length (predominantly males with regenerated tails) and relatively thinner tail base experienced higher infestation rates. In turn, relatively heavier females for their snout-vent length were less tick infested. Although some components of throat and chest coloration varied significantly with relative tail length, tail-base thickness, body mass, and head size, a measure of male throat and female chest color saturation seemed independent of lizard morphology. After correcting for the effects of morphology on skin coloration and tick load, the saturation of blue throat color in male lizards decreased with increasing level of tick infestation. In contrast, yellow chest color saturation increased with residual tick numbers in females. Considering presumably different signaling functions of male and female lizard coloration, our work suggests that tick infestation might represent a handicap for Green Lizards.
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One of the most extensively investigated sexually selected phenotypic characters is coloration. A knowledge of individual variation in the anatomical basis of coloration is essential for better understanding of the link between colour expression and its information content. We investigated the association of great tit (Parus major) black crown feather structure and coloration [brightness, ultraviolet (UV) chroma] at the individual level, using transmission electron microscopic, photographic and spectrometric techniques. We quantified feather structure at three different levels of spatial organization [feather macrostructure (barb and barbule density), barb nanostructure (melanin density and cortex thickness) and barbule nanostructure (melanin discontinuity, melanin density and cortex thickness)]. Macrostructure and barbule and barb nanostructure explained sex differences in reflectance. Regardless of sex, brightness changed with barb density, and UV chroma changed with barbule melanin density and macrostructure. Only among males, brightness was related to barbule melanin density and barb cortex thickness, and UV chroma was associated with melanin discontinuity, barbule cortex thickness and barb melanin density. Our results show that individual differences in plumage colour are determined at multiple hierarchical levels of feather structural organization.
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Hormones can mediate suites of correlated traits. Melanocortins regulate melanin synthesis and elements of the melanocortin system can directly, and indirectly, affect a number of other traits, such as stress reactivity. Trait correlation in with the melanocortin system have been studied mainly in birds and mammals but less so in reptiles. We examined adult male western fence lizards (Sceloporus occidentalis) and if melanization was correlated with plasma levels of three hormones, including peptide hormone α-melanocyte stimulating hormone (α-MSH), testosterone and corticosterone, and ectoparasite loads. This lizard is darker at higher elevations in California, and we compared five high-elevation and four low-elevation populations during comparable periods of the breeding season at each site. We first validated use of an α-MSH assay kit with lizard plasma. Since Anolis carolinensis is one of the few species with published values for α-MSH plasma levels, we assayed both Anolis and Sceloporus plasma and compared hormone values to those we generated for Anolis to the publish values. We also evaluated effects of different methods of storing spiked plasma pools on resulting α-MSH concentrations. Plasma levels of α-MSH did not differ significantly, but some populations differed significantly in mean corticosterone and mean testosterone. Combining all individuals from the nine populations, we found that individual variation in α-MSH was not associated with individual variation in melanization, but levels of α-MSH were positively associated with plasma testosterone and negatively associated with corticosterone. The lack of association between individual levels of melanization and expression of most other traits differs from a growing number of within-population studies of melanization, and we discuss what differences in physiological mechanisms could produce different hypothetical patterns. Circulating levels of -MSH are only one element of the melanocortin system; in situ synthesis of α-MSH by the skin and the diversity of melanocortin receptors could also contribute to variation in traits mediated by the melanocortin system and should be examined.
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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.
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In the context of the immunocompetence handicap hypothesis, we explored how differences in parasite load affect the way in which sexual ornaments codify information about individual quality. We studied variation in sexual signals in two Iberian populations of the lizard Psammodromus algirus, a species in which sexually active males display a red head coloration. In one population, males were free of tick nymphs, whereas in the other one all males were tick-infested (mean of 12.7 tick nymphs/individual).At the onset of the breeding season, the red-coloured surface was larger in the non-parasitized population than in the parasitized one, whereas the opposite was true for colour saturation. We experimentally simulated a bacterial infection (by intraperitoneal injection of lipopolysaccharide) to examine the effects of immune activation on the expression of this sexual ornament. In the non-parasitized population, our treatment caused a reduction in the red-coloured surface of experimental males, whereas in the parasitized population it caused a decrease in colour saturation. In the parasitized population, males that displayed sexual coloration were larger, and had fewer parasites, than uncoloured ones, and inflammatory response to lipopolysaccharide injection in the palm of the hind paw was negatively correlated with colour saturation, but not with colour extension. Thus, we suggest parasites not only constrained the expression of sexual ornaments, but they also changed the signal properties that conveyed useful information about the quality of their bearers.
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Male Eumeces laticeps develop bright orange head coloration during the spring breeding season, when they fight with other males and engage in sexual behavior with females. Outside the breeding season the head color fades and the sexual and agonistic behaviors cease. Intraperitoneal implantation of testosterone propionate in Silastic capsules restores the bright orange head coloration and activates courtship and agonistic behaviors in castrated males.
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Conspicuous displays of color comprise an enormously diverse and functionally complex class of biological signals. Many of these displays are widely publicized as resulting from chemical colorants known as pigments, which act by selectively "absorbing" part of the light spectrum (Appendix 1). However, the full diversity of animal coloration is just as strongly influenced by optically active surface structures, which act by selectively "reflecting" light (i.e., scattering). In cases where light is scattered coherently, these structural colors produce displays that are often metallic, iridescent, or kaleidoscopic in appearance. In addition to structural coloration, mechanisms such as bioluminescence and fluorescence allow the actual creation of colored light, thereby transcending the simple reflectance of whatever ambient wavelengths are available. There is enormous variation among all of these classes of colorants, and most signals arise through the interaction of diverse suites of pigments and reflecting (structural) mechanisms. Despite this complexity, however, the field of behavioral ecology has been largely preoccupied with understanding how carotenoids-a single group of pigments-may broker the honest signaling of individual quality. This focus has proven highly productive in many respects, but it has also fostered a limited and overly simplistic view of how color signals really work. As we outline here, the complete emerging story of animal coloration is far more complex and interesting.
Article
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.
Article
The Hamilton & Zuk (1982) hypothesis of parasite-mediated sexual selection has been the subject of both inter- and intraspecific tests. Past reviews have used vote counting to determine whether this hypothesis is supported by empirical evidence. This study reanalysed 199 separate quantitative assessments of a central prediction of the Hamilton & Zuk hypothesis using meta-analytical techniques. Overall, our meta-analysis showed that there was a significant negative effect of parasites on male showiness as predicted. However the magnitude of this effect varied between host taxa and between endo and ectoparasitic taxa. As a whole intraspecific correlations between parasite load and male showiness provided very little support for the hypothesis with only the effect of parasites on fish morphology matching the Hamilton & Zuk prediction. There was more support for the hypothesis from interspecific studies especially those based upon the original Hamilton & Zuk (1982) data set, although other bird studies provided weaker support. The generality of the Hamilton & Zuk hypothesis in respect to parasite mediated sexual selection across taxa is thrown into doubt by these results. However, in some specific host-parasite systems the role of parasites appears important and future intraspecific tests of parasite-mediated sexual selection should perhaps focus on such systems.
Article
Sexual selection has been invoked as a major force in the evolution of secondary sexual traits, including sexually dimorphic colorations. For example, previous studies have shown that display complexity and elaborate ornamentation in lizards are associated with variables that reflect the intensity of intrasexual selection. However, these studies have relied on techniques of colour analysis based on human – rather than lizard – visual perception. Here, we use reflectance spectrophotometry and visual modelling to quantify sexual dichromatism considering the overall colour patterns of lacertids, a lizard clade in which visual signalling has traditionally been underrated. These objective methods of colour analysis reveal a large, previously unreported, degree of sexual dichromatism in lacertids. Using a comparative phylogenetic approach, we further demonstrate that sexual dichromatism is positively associated with body size dimorphism (an index of intrasexual selection), suggesting that conspicuous coloration in male lacertids has evolved to improve opponent assessment under conditions of intense male–male competition. Our findings provide the first evidence for the covariation of sexual dichromatism and sexual size dimorphism in lacertids and suggest that the prevalent role of intrasexual selection in the evolution of ornamental coloration is not restricted to the iguanian lineage, but rather may be a general trend common to many diurnal lizards.
Article
Life-history theory predicts that there is a trade-off between reproductive effort and several traits that determine fitness. Infectious disease has gained acceptance as a crucial Factor linking both variables. In most instances phenotypic manipulation is necessary to convincingly demonstrate a causal relationship of reproductive effort on parasitism. However, experimental studies that manipulate reproductive effort or parasite load have been rarely conducted in reptiles. In this study, we manipulated reproductive effort of male lizards (Psammodromus algirus) through testosterone implants, and measured the associated response in some haematological variables and parasite load. Testosterone-supplemented males had lower scores than control males in factor 1 of a PCA for different blood parameters. This factor is correlated with the number of white blood cells, especially lymphocytes, and with plasma glucose levels. Experimental males also had higher scores in factor 3 that is mainly related to protein catabolism. Scores of males in component 1 tended to be correlated negatively with tick load, while scores in component 3 were correlated positively with the number of haemogregarines in the blood. These results suggest that higher investment in reproduction decreases the immune defences, and conduces to the use of structural resources, which may render individuals more susceptible to some haemoparasites. This is consistent with the idea that an increase in reproductive effort mediated by testosterone has a negative effect on the ability to counteract parasite infections.
Article
Phrynosomatid lizards show considerable variation among species in the occurrence of a secondary sexual trait, blue abdominal coloration. The production of blue skin may be controlled by at least two cellular components, melanin in melanophores, and guanine in iridophores. To examine the hypothesis that a mechanism producing variation in abdominal coloration is variation in the presence of melanin in the melanophores within the dermal layer of skin, we used light microscopy to compare melanin density of five species of phrynosomatid lizards with ancestral and derived abdominal coloration. Our results show that the skin of adults with blue abdominal coloration has more dermal melanin than white skin regardless of species or sex. We experimentally tested this relationship by examining the dermal melanin in skin from female Sceloporus undulatus consobrinus with exogenously elevated levels of testosterone or 5α-dihydrotestosterone. These females displayed malelike abdominal coloration and malelike melanin density. Our results suggest that melanin density plays a role in the presence of blue abdominal coloration in these phrynosomatid lizards.
Article
MANY species exhibit colour polymorphisms associated with alternative male reproductive strategies, including territorial males and 'sneaker males' that behave and look like females1-3. The prevalence of multiple morphs is a challenge to evolutionary theory because a single strategy should prevail unless morphs have exactly equal fitness4,5 or a fitness advantage when rare6,7. We report here the application of an evolutionary stable strategy model to a three-morph mating system in the side-blotched lizard. Using parameter estimates from field data, the model predicted oscillations in morph frequency, and the frequencies of the three male morphs were found to oscillate over a six-year period in the field. The fitnesses of each morph relative to other morphs were non-transitive in that each morph could invade another morph when rare, but was itself invadable by another morph when common. Concordance between frequency-dependent selection and the among-year changes in morph fitnesses suggest that male interactions drive a dynamic 'rock-paper-scissors' game7.
Article
Intraspecific colour variation is common in nature and can vary from the coexistence of discrete colour variants in polymorphic species to continuous variation. Whether coloration is continuous or discrete is often ambiguous and many species exhibit a combination of the two. The nature of the variation (discrete or continuous) has implications for both the genetic basis of the colour variation and the evolutionary processes generating and maintaining it. Consequently, it is important to qualify the existence of discrete morphs, particularly in relation to the animal's visual system. In this study, we quantified male throat colour variation in Ctenophorus decresii tawny dragon lizard and tested for morphological and ecological correlates of the colour variants. We confirmed that discrete throat colour morphs can be defined based on colour and pattern analyses independent of the human visual system. We also found that the colour variants differed in their conspicuousness from the background, to the lizard's visual system, which has implications for signalling. However, the morphs did not differ in morphology or microhabitat use, which suggests that these characteristics are not involved in the evolutionary maintenance of the polymorphism.
Article
Male secondary sexual traits purportedly facilitate female choice of a potential mate's quality. One example of male quality is the ability to resist detrimental infections by parasites; sexual traits that reflect parasite infection can allow females to select for parasite resistance in future offspring. High parasite numbers can constrain the exaggeration of male traits, but few studies have examined the effects of parasites on female secondary traits. Female Mexican boulder spiny lizards Sceloporus pyrocephalus, undergo a change in secondary sexual coloration over their breeding season and express red gular regions and gray gular stripes in association with late stages of follicle maturation during the reproductive cycle, as well as blue ventral stripes. We examined if color change associated with the female reproductive cycle varied in hue, saturation and brightness in relation to high nematode loads. Our results suggest that high nematode loads of particular areas of the body are correlated with dull, as opposed to bright, secondary sexual coloration in females of S. pyrocephalus. One reason females could be most vulnerable to nematodes during late reproductive stages is because of corresponding high concentrations of circulating testosterone known to occur in this species at this time. Testosterone has demonstrated immunosuppressive effects in many species; however, results have varied and conclusive evidence for its role in immune function remains controversial. Using a subset of individuals from this study, we found that high concentrations of plasma testosterone were significantly related to high nematode loads. These findings prompt further studies examining the physiological attributes of parasite infestation, the honest signaling capabilities of nematode loads and their potential role in sexual selection for coloration in females.
Article
The mechanisms responsible for the explosive radiations of haplochromine cichlid fishes in Africa's great lakes remain controversial. Since species thought to be closely related often differ most apparendy in male breeding colours, I examined patterns of male colour variation in rock-dwelling cichlids from Lake Malawi to test whether initial divergence between species is likely to have been caused by adaptation to differing habitats, by selection against hybridization (reinforcement or character displacement), or by sexual selection. I found that all significant variation in overall male colour occurs within, not between, species complexes, in contrast to variation in habitat and behavioural traits, which differed significandy between complexes. Male colour does not vary significandy with habitat characteristics such as water depth, and sympatric species differ no more in colour than allopatric ones. These results fail to provide support for adaptation or reinforcement as initial causes of colour divergence, and are consistent with the possibility that divergence may instead have been caused by sexual selection, but a direct test of sexual selection is not yet possible.