Negative Association Between Conspicuous Visual Display and Chemosensory Behavior in Two Phrynosomatid Lizards

Communication in one sensory modality can influence communication in others. Lizards in many phrynosomatid species use primarily visual but also chemical signals. The striped plateau lizard, Sceloporus virgatus , exhibits evolutionary loss of a male color signal that in many species is used during aggressive postural displays towards conspecific males. These patches are used similarly in Urosaurus , the sister genus to Sceloporus . We compared a species in which a color signal has been lost, S. virgatus , to a species retaining the ancestral character state of blue abdominal display patches, Urosaurus ornatus , the common tree lizard, to test two hypotheses: (i) conspicuous postural displays that reveal the abdominal patch location are used less in the species that has lost the color patches; and (ii) potential chemical signals are used more in the species with the color loss. We analyzed both visual display behavior (push-up, full-show) and chemosensory behavior (tongue flick and nose tap) of male lizards following their introduction to a resident conspecific male in his home terrarium. Resident males performed very low rates of all behaviors, but intruders exhibited sufficient behavior for analysis.
Supporting the first hypothesis, S. virgatus were less likely than U. ornatus to perform full-show, a display that reveals abdominal skin. Male S. virgatus were more likely to perform push-up than U. ornatus , although S. virgatus performed push-up infrequently. Push-up is a postural display that does not specifically reveal the abdominal patch location. Supporting the second hypothesis, S . virgatus were more likely to perform chemosensory behaviors and performed them at a greater rate than did U. ornatus . Work comparing more closely related species is warranted to determine whether a negative association between conspicuous visual displays and chemosensory behavior is a general pattern.     

Does spatial variation in predation pressure modulate selection for aposematism?

It is widely believed that aposematic signals should be conspicuous, but in nature, they vary from highly conspicuous to near cryptic. Current theory, including the honest signal or trade‐off hypotheses of the toxicity–conspicuousness relationship, cannot explain why adequately toxic species vary substantially in their conspicuousness. Through a study of similarly toxic Danainae (Nymphalidae) butterflies and their mimics that vary remarkably in their conspicuousness, we show that the benefits of conspicuousness vary along a gradient of predation pressure. Highly conspicuous butterflies experienced lower avian attack rates when background predation pressure was low, but attack rates increased rapidly as background predation pressure increased. Conversely, the least conspicuous butterflies experienced higher attack rates at low predation pressures, but at high predation pressures, they appeared to benefit from crypsis. Attack rates of intermediately conspicuous butterflies remained moderate and constant along the predation pressure gradient. Mimics had a similar pattern but higher attack rates than their models and mimics tended to imitate the signal of less attacked model species along the predation pressure gradient. Predation pressure modulated signal fitness provides a possible mechanism for the maintenance of variation in conspicuousness of aposematic signals, as well as the initial survival of conspicuous signals in cryptic populations in the process of aposematic signal evolution, and an alternative explanation for the evolutionary gain and loss of mimicry.     

Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish

The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.     

Reflectance of sexually dichromatic UV‐blue patches varies during the breeding season and between two subspecies of Gallotia galloti (Squamata: Lacertidae)

Body coloration is sexually dimorphic in many vertebrate species, including lizards, in which males are often more conspicuous than females. A detailed analysis of the relative size of coloured patches and their reflectance, including the ultraviolet (UV) range, has rarely been performed. In the present work we quantified sexual dimorphism in body traits and surface area of all lateral patches from adult females and males of two subspecies of Gallotia galloti (G. g. galloti and G. g. eisentrauti). We also analysed the magnitude of sexual dichromatism in the UV‐visible reflectance of such patches and the changes in patch size and brightness during the reproductive season (April–July). Males had significantly larger patch areas (relative to their snout‐vent length) and higher brightness (mainly in the UV‐blue range) than did females in both subspecies. The comparison of relative patch areas among months did not reach statistical significance. However, patch brightness significantly changed during the breeding season: that of the UV‐blue (300–495 nm) range from lizards of the two subspecies was significantly larger in June than in April, while brightness in the 495–700 nm range in G. g. galloti was larger in May, June, and July than in April. A different pattern of dichromatism was also detected in the two populations, with G. g. eisentrauti being more sexually dichromatic than G. g. galloti. We discuss the results in terms of possible evolutionary causes for the sexual dichromatism related to different ecological characteristics of the habitats where each subspecies live. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 556–569.     

Ultraviolet sexual dimorphism and assortative mating in blue tits

In spite of strong evidence for viability-based sexual selection and sex ratio adjustments, the blue tit, Parus caeruleus, is regarded as nearly sexually monomorphic and no epigamic signals have been found. The plumage coloration has not, however, been studied in relation to bird vision, which extends to the UV-A waveband (320 to 400 nm). Using molecular sex determination and UV/VIS spectrometry, we report here that blue tits are sexually dichromatic in UV/blue spectral purity (chroma) of the brilliant crown patch. It is displayed in courtship by horizontal posturing and erected nape feathers. A previously undescribed sexual dimorphism in crown size (controlling for body size) further supports its role as an epigamic ornament. Against grey-brown leaf litter and bark during pair formation in early spring, but also against green vegetation, UV contributes strongly to conspicuousness and sexual dimorphism. This should be further enhanced by the UV/bluish early morning skylight (''woodland shade'') in which blue tits display. Among 18 breeding pairs, there was strong assortative mating with respect to UV chroma, but not size, of the crown ornament. We conclude that blue tits are markedly sex dimorphic in their own visual world, and that UV/violet coloration probably plays a role in blue tit mate acquisition.     

Phenotypic plasticity drives a depth gradient in male conspicuousness in threespine stickleback,Gasterosteus aculeatus

Signal evolution is thought to depend on both a signal's detectability or conspicuousness (signal design) as well as any extractable information it may convey to a potential receiver (signal content). While theoretical and empirical work in sexual selection has largely focused on signal content, there has been a steady accrual of evidence that signal design is also important for trait evolution. Despite this, relatively little attention has been paid to spatial variation in the conspicuousness of a given signal, especially over small spatial scales (relative to an organism's dispersal distance). Here, we show that visual signals of male threespine stickleback vary in conspicuousness, depending on a male's nest depth within a given lake. Deeper nesting males were typically more chromatically conspicuous than shallow nesting males. This trend is partly because all male stickleback are more conspicuous in deep optical environments. However, deep males are even more conspicuous than environmentally driven null expectations, while shallow males tend to be disproportionally cryptic. Experimental manipulation of male nesting depth induced plastic changes in nuptial color that replicated the natural gradients in conspicuousness. We discuss a number of potential mechanisms that could produce depth gradients in conspicuousness in male stickleback, including concomitant depth gradients in diet, predation pressure, male/female density, female preference, and opportunity for sexual selection.     

Conspicuousness of Dickerson's collared lizard (Crotaphytus dickersonae) through the eyes of conspecifics and predators

Selection should favour coloration in organisms that is more conspicuous to their own visual system than to those of their predators or prey. We tested this prediction in Dickerson's collared lizard ( Crotaphytus dickersonae ), a sexually dichromatic desert reptile that preys on insects and smaller lizard species, and which in turn is prey for birds and snakes. We modelled the spectral sensitivities of the lizards and their avian and snake predators, and compared the conspicuousness of the lizards' entire colour patterns with each class of viewers. Almost all comparisons involving females strongly supported our prediction for greater chromatic and brightness conspicuousness against local terrestrial visual backgrounds to their own modelled visual system than to those of avian and snake predators. Males, in contrast, exhibited far fewer cases of greater conspicuousness to their own visual system than to those of their predators. Our own perception of spectral similarity between blue C. dickersonae males and a local nonterrestrial visual background (i.e. the Sea of Cortéz) prompted a further investigation. We compared sea (and sky) radiance with dorsum radiance of C. dickersonae males and with males from two distantly-related Crotaphytus collaris populations in which males possess blue bodies. In all three visual models, C. dickersonae males exhibited significantly lower chromatic contrast with the sea (and sky) than did their noncoastal, blue-bodied congeners. Among potential explanations, the blue body coloration that is unique to male C. dickersonae may offset, if only slightly, the cost of visibility to predators (and to prey) through reduced contrast against the extensive, local, nonterrestrial blue backgrounds of the sea and sky.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 749–765.     

Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards

The evolution of conspicuous male display ornaments is a common trend in diverse groups of organisms and a continuing challenge to studies of sexual selection. A phylogenetic approach was used to examine macro-evolutionary patterns of change in sexually dichromatic display coloration (distinctively coloured belly patches) among 130 taxa of phrynosomatid lizards. The results showed repeated losses of sexual dimorphism, which occur through losses of conspicuous male coloration or gains of conspicuous female coloration. The frequent loss of male traits is surprising, given that sexual selection presumably drives their evolutionary origin and maintenance, but is consistent with a recently proposed hypothesis suggesting that females may lose responsiveness to male traits over macro-evolutionary time-scales. The observation of repeated losses of male traits in phrynosomatid lizards (and other groups) may have implications for testing among competing models for the evolution of female preferences. A concentrated changes test showed that changes in male display coloration are significantly associated with the use of ground-dwelling habitat, as opposed to rock- or tree-dwelling habitats. This result suggests a role for natural selection in the loss of male display traits in phrynosomatid lizards, but habitat type alone may be insufficient to explain these losses.     

Evolution of sexual dichromatism in relation to nesting habits in European passerines: a test of Wallace's hypothesis

Wallace proposed in 1868 that natural rather than sexual selection could explain the striking differences in avian plumage dichromatism. Thus, he predicted that nesting habits, through their association with nest predation, could drive changes in sexual dichromatism by enabling females in cavity nesters to become as conspicuous as males, whereas Darwin (1871, The Descent of Man and Selection in Relation to Sex, John Murray, London) argued that sexual selection was the sole explanation for dichromatism. Sexual dichromatism is currently used as indicating the strength of sexual selection, and therefore testing Wallace's claim with modern phylogentically controlled methodologies is of prime interest for comparing the roles of natural and sexual selection in affecting the evolution of avian coloration. Here, we have related information on nest attendance, sexual dichromatism and nesting habits (open and cavity nesting) to male and female plumage conspicuousness in European passerines. Nest incubation attendance does not explain male or female plumage conspicuousness but nest type does. Moreover, although females of monochromatic and cavity nesting species are more conspicuous than females of other species, males of monochromatic and open nesting species are those with more cryptic plumage. Finally, analyses of character evolution suggest that changes in nesting habits influence the probability of changes in both dichromatism and plumage conspicuousness of males but do not significantly affect those in females. These results strongly suggest a role of nesting habits in the evolution of plumage conspicuousness of males, and a role for sexual selection also in females, both factors affecting the evolution of sexual dichromatism. We discuss our findings in relation to the debate that Darwin and Wallace maintained more than one century ago on the importance of natural and sexual selection in driving the evolution of plumage conspicuousness and sexual dichromatism in birds, and conclude that our results partly support the evolutionary scenarios envisaged by both extraordinary scientists.     

Conspicuous visual signals do not coevolve with increased body size in marine sea slugs

Many taxa use conspicuous colouration to attract mates, signal chemical defences (aposematism) or for thermoregulation. Conspicuousness is a key feature of aposematic signals, and experimental evidence suggests that predators avoid conspicuous prey more readily when they exhibit larger body size and/or pattern elements. Aposematic prey species may therefore evolve a larger body size due to predatory selection pressures, or alternatively, larger prey species may be more likely to evolve aposematic colouration. Therefore, a positive correlation between conspicuousness and body size should exist. Here, we investigated whether there was a phylogenetic correlation between the conspicuousness of animal patterns and body size using an intriguing, understudied model system to examine questions on the evolution of animal signals, namely nudibranchs (opisthobranch molluscs). We also used new ways to compare animal patterns quantitatively with their background habitat in terms of intensity variance and spatial frequency power spectra. In studies of aposematism, conspicuousness is usually quantified using the spectral contrast of animal colour patches against its background; however, other components of visual signals, such as pattern, luminance and spectral sensitivities of potential observers, are largely ignored. Contrary to our prediction, we found that the conspicuousness of body patterns in over 70 nudibranch species decreased as body size increased, indicating that crypsis was not limited to a smaller body size. Therefore, alternative selective pressures on body size and development of colour patterns, other than those inflicted by visual hunting predators, may act more strongly on the evolution of aposematism in nudibranch molluscs.     

Evolution of color variation in dragon lizards: quantitative tests of the role of crypsis and local adaptation

Abstract Many animal species display striking color differences with respect to geographic location, sex, and body region. Traditional adaptive explanations for such complex patterns invoke an interaction between selection for conspicuous signals and natural selection for crypsis. Although there is now a substantial body of evidence supporting the role of sexual selection for signaling functions, quantitative studies of crypsis remain comparatively rare. Here, we combine objective measures of coloration with information on predator visual sensitivities to study the role of crypsis in the evolution of color variation in an Australian lizard species complex (Ctenophorus decresii). We apply a model that allows us to quantify crypsis in terms of the visual contrast of the lizards against their natural backgrounds, as perceived by potential avian predators. We then use these quantitative estimates of crypsis to answer the following questions. Are there significant differences in crypsis conspicuousness among populations? Are there significant differences in crypsis conspicuousness between the sexes? Are body regions “exposed” to visual predators more cryptic than “hidden” body regions? Is there evidence for local adaptation with respect to crypsis against different substrates? In general, our results confirmed that there are real differences in crypsis conspicuousness both between populations and between sexes; that exposed body regions were significantly more cryptic than hidden ones, particularly in females; and that females, but not males, are more cryptic against their own local background than against the background of other populations. Body regions that varied most in contrast between the sexes and between populations were also most conspicuous and are emphasized by males during social and sexual signaling. However, results varied with respect to the aspect of coloration studied. Results based on chromatic contrast (“hue’ of color) provided better support for the crypsis hypothesis than did results based on achromatic contrast (“brightness’ of color). Taken together, these results support the view that crypsis plays a substantial role in the evolution of color variation and that color patterns represent a balance between the need for conspicuousness for signaling and the need for crypsis to avoid predation.     

Does reproductive mode affect sexually-selected coloration? Evaluating UV-blue spots in parthenogenetic and bisexual lizards of the genus Darevskia

Sexual selection often leads to evolution of conspicuous signals, raising the chances of attracting not only potential mates, but also predators. In lacertid lizards, ultraviolet (UV)–blue spots on flanks and shoulders represent such a trait. Some level of correlation between male and female ornamentation is also known to exist. Therefore, the phenotype of females may change in the absence of sexual selection. We tested this hypothesis on a complex of parthenogenetic and bisexual lizards of the genus Darevskia. We evaluated area, counts, and chromatic properties (UV opponency, saturation) of UV–blue spots and compared the values between the clones and their bisexual progenitor species. We found a fair heterogeneity between the parthenogenetic species, but no general tendency toward higher crypsis or conspicuousness. Values of the parthenogens were not significantly different from the values of sexual females. A possible explanation is that the changes in selective forces associated with parthenogenetic reproduction are too small to affect the resulting pattern of selective pressures on the studied traits, or that the phenotypes of the parthenogens result from the unique combination of parental genomes and are conserved by clonal reproduction.     

Influence of ambient light on the evolution of colour signals: comparative analysis of a Neotropical rainforest bird community

Rainforests offer two contrasted light environments: a bright canopy rich in blue and UV and a dark understorey, rich in green and orange. Therefore, natural selection for crypsis should favour dark brown signals in understorey and bright green signals in canopy, whereas sexual selection for conspicuousness should favour bright yellow‐red signals in understorey and dark blue and UV signals in canopy. Using spectrometry and comparative analyses, we examined the relationship between ambient light and colour signals in a bird community of French Guiana. It appears that brightness and hue are mostly naturally selected, while UV content of plumage is more likely sexually selected. At each height, both sexes present similar coloration but males display more conspicuous sexually selected patterns than females. These results show that ambient light drives the evolution of colour signals at community scale, and should be considered when studying signalling in other communities and light‐contrasted ecosystems.     

Conspicuousness is correlated with toxicity in marine opisthobranchs

Aposematism is defined as the use of conspicuous colouration to warn predators that an individual is chemically or otherwise defended. Mechanisms that drive the evolution of aposematism are complex. Theoretical and empirical studies show that conspicuousness can be either positively or negatively correlated with toxicity as once aposematism is established, species can allocate resources into becoming more conspicuous and/or increase secondary defences. Here, we investigated the evolution of conspicuousness and toxicity in marine opisthobranchs. Conspicuousness of colour signals was assessed using spectral reflectance measurements and theoretical vision models from the perspective of two reef fish signal receivers. The relative toxicity of chemicals extracted from each opisthobranch species was then determined using toxicity assays. Using a phylogenetic comparative analysis, we found a significant correlation between conspicuousness and toxicity, indicating that conspicuousness acts as an honest signal when signifying level of defence and provides evidence for aposematism in opisthobranchs.     

Environment-contingent sexual selection in a colour polymorphic fish

Sexual selection could be a driving force in the maintenance of intraspecific variation, but supporting observations from nature are limited. Here, we test the hypothesis that spatial heterogeneity of the visual environment can influence sexual selection on colourful male secondary traits such that selective advantage is environment contingent. Using a small fish endemic to Sulawesi, Indonesia (Telmatherina sarasinorum) that has five male colour morphs varying in frequency between two visually distinct mating habitats, we used direct behavioural observations to test the environment-contingent selection hypothesis. These observations were combined with measurements of the visual environment, fish coloration and the sensitivity of visual photopigments to determine whether differential morph conspicuousness was associated with reproductive success across habitats. We found that blue and yellow males are most conspicuous in different habitats, where they also have the highest reproductive fitness. A less conspicuous grey morph also gained high reproductive success in both habitats, raising the possibility that alternative behaviours may also contribute to reproductive success. In a comprehensive analysis, conspicuousness was strongly correlated with reproductive success across morphs and environments. Our results suggest an important role for spatially heterogeneous environments in the maintenance of male colour polymorphism.     

Identifying the ecological conditions that select for intermediate levels of aposematic signalling

Chemically defended species often have conspicuous signals that warn potential predators of these defences. Recent evidence suggests that some such aposematic prey are not as conspicuous as possible, even though increased conspicuousness would bring additional anti-predator benefits. Here we present a simple model to explore the generality of these observations. Our model predicts that optimal fitness will often be achieved at an intermediate level of conspicuousness and not simply by maximising conspicuousness. This comes about because of the ubiquitous trade-off that increased conspicuousness has an ecological cost in increasing the encounter rate with predators, as well as a benefit in terms of enhancing learned aversion by predators of defended prey. However, importantly, we also predict that a small deviation away from maximal crypsis generally causes a decrease in fitness, even if a larger deviation would lead to an intermediate level of conspicuousness that maximises fitness. Hence, further consideration of whether intermediate levels of aposematism are as common in nature as predicted in this model will require consideration of the underlying evolution of appearance, and the plausibility of evolution across the fitness trough, from maximal crypsis to an intermediate level of aposematism.     

COARSE DARK PATTERNING FUNCTIONALLY CONSTRAINS ADAPTIVE SHIFTS FROM APOSEMATISM TO CRYPSIS IN STRAWBERRY POISON FROGS

Ecological specialization often requires tight coevolution of several traits, which may constrain future evolutionary pathways and make species more prone to extinction. Aposematism and crypsis represent two specialized adaptations to avoid predation. We tested whether the combined effects of color and pattern on prey conspicuousness functionally constrain or facilitate shifts between these two adaptations. We combined data from 17 natural populations of strawberry poison frogs, Oophaga pumilio with an experimental approach using digitalized images of frogs and chickens as predators. We show that bright coloration often co‐occurs with coarse patterning among the natural populations. Dull green frogs with coarse patterning are rare in nature but in the experiment they were as easily detected as bright red frogs suggesting that this trait combination represents a transient evolutionary state toward aposematism. Hence, a gain of either bright color or coarse patterning leads to conspicuousness, but a transition back to crypsis would be functionally constrained in populations with both bright color and coarse patterning by requiring simultaneous changes in two traits. Thus, populations (or species) signaling aposematism by conspicuous color should be less likely to face an evolutionary dead end and more likely to radiate than populations with both conspicuous color and coarse patterning.     

Conspicuousness, not colour as foraging cue in plant–animal signalling

The global prevalence of red and black fruits has still not been explained. Hypotheses based on innate consumer preferences have been tested and rejected. Though colour itself plays an important role in animal foraging, it is only one component of signals. Another major component are colour contrasts against background achieving the conspicuousness of signals. In order to evaluate which signal component determines consumers behaviour, we measured fruit colour and colour contrasts of 43 species against their natural background under ambient light conditions. Red and black fruits exhibit stronger contrasts and are therefore more conspicuous to consumers than fruits of other colours. Subsequently, trials were carried out to determine whether colour or conspicuousness influences avian food choice. Four bird species strongly preferred contrasting red–green or black–green over uni-coloured red, green, or black fruit displays, while no preference for particular hues was found. We therefore hypothesize that conspicuousness determines avian food selection and define the contrast hypothesis: Diurnal dispersers select fruit colours based on their conspicuousness and not their colour itself.
Because colour vision is an ancient trait, the entire heterogeneous group of frugivorous birds most likely perceives conspicuousness uniformly over evolutionary time spans. Conspicuousness has thus the potential to explain the global prevalence of red and black fruits.