What determines dewlap diversity in Anolis lizards? An among‐island comparison

Animal signalling systems are extremely diverse as they are under different, often conflicting, selective pressures. A classic textbook example of a diverse signal is the anoline dewlap. Both at the inter‐ and intraspecific levels, dewlap size, colour, shape and pattern vary extensively. Here, we attempt to elucidate the various factors explaining the diversity in dewlap size and pattern among seven Anolis sagrei populations from different islands in the Bahamas. The seven islands differ in the surface area, number and kind of predators, sexual size dimorphism and Anolis species composition. In addition, we investigate whether selective pressures acting on dewlap design differ between males and females. Whereas dewlap pattern appears to serve a role in species recognition in both sexes, our data suggest that relative dewlap size is under natural and/or sexual selection. We find evidence for the role of the dewlap as a pursuit‐deterrence signal in both males and females as relative dewlap size is larger on islands where A. sagrei occurs sympatrically with predatory Leiocephalus lizards. Additionally, in males relatively large dewlaps seem to be selected for in a sexual context, whereas in females natural selection, for instance by other predators than Leiocephalus lizards, appears to constrain relative dewlap size.     

Climate‐related environmental variation in a visual signalling device: the male and female dewlap in Anolis sagrei lizards

Animals communicate using a variety of signals that differ dramatically among and within species. The astonishing dewlap diversity in anoles has attracted considerable attention in this respect. Yet, the evolutionary processes behind it remain elusive and have mostly been explored for males only. Here, we considered Anolis sagrei males and females to study signal divergence among populations. First, we assessed the degree of variation in dewlap design (size, pattern and colour) and displays by comparing 17 populations distributed across the Caribbean. Second, we assessed whether the observed dewlap diversity is associated with variation in climate‐related environmental conditions. Results showed that populations differed in all dewlap characteristics, with the exception of display rate in females. We further found that males and females occurring in ‘xeric’ environments had a higher proportion of solid dewlaps with higher UV reflectance. In addition, lizards inhabiting ‘mesic’ environments had primarily marginal dewlaps showing high reflectance in red. For dewlap display, a correlation with environment was only observed in males. Our study provides evidence for a strong relationship between signal design and prevailing environmental conditions, which may result from differential selection on signal efficacy. Moreover, our study highlights the importance of including females when studying dewlaps in an evolutionary context.     

The evolution of performance-based male fighting ability in Caribbean Anolis lizards

Despite the empirical and theoretical attention paid to the role of sexual signals in resolving agonistic interactions between conspecific males, few studies have applied a comparative perspective, particularly across species that vary in combat intensity. We investigated the relative roles of a male sexual signal (dewlap size) and whole-organism performance capacity (bite force) on male combat outcomes in nine species of Caribbean Anolis lizards that differ markedly in territoriality, as indicated by sexual size dimorphism. We found that (1) dewlap size was generally an honest signal of bite force in dimorphic but not less dimorphic species; (2) maximum bite force consistently predicted male combat success in dimorphic but not less dimorphic species; (3) in contrast to a priori predictions, dewlap size significantly predicted male combat success in less dimorphic but not dimorphic species; and (4) the incidence of biting but not dewlapping increases as species become more dimorphic. These findings suggest that more dimorphic (and hence more territorial) species escalate to biting during fights more readily compared with less territorial species. The ecological and behavioral qualities of species may therefore modify both the shape and the size of sexually selected traits as well as the nature of the information those traits convey.     

The incredible shrinking dewlap: signal size,skin elasticity,and mechanical design in the green anole lizard (Anolis carolinensis)

The expression of male secondary sexual traits can be dynamic, changing size, shape, color, or structure over the course of different seasons. However, the factors underlying such changes are poorly understood. In male Anolis carolinensis lizards, a morphological secondary sexual signal called the dewlap changes size seasonally within individuals. Here, we test the hypothesis that seasonal changes in male dewlap size are driven by increased use and extension of the dewlap in spring and summer, when males are breeding, relative to the winter and fall. We captured male green anole lizards prior to the onset of breeding and constrained the dewlap in half of them such that it could not be extended. We then measured dewlap area in the spring, summer, and winter, and dewlap skin and belly skin elasticity in summer and winter. Dewlaps in unconstrained males increase in area from spring to summer and then shrink in the winter, whereas the dewlaps of constrained males consistently shrink from spring to winter. Dewlap skin is significantly more elastic than belly skin, and skin overall is more elastic in the summer relative to winter. These results show that seasonal changes in dewlap size are a function of skin elasticity and display frequency, and suggest that the mechanical properties of signaling structures can have important implications for signal evolution and design.     

Evolution of the ungulate dewlap: thermoregulation rather than sexual selection or predator deterrence?

Background

Dewlaps are iconic features of several ungulate species and, although a role in signalling has been postulated, their function remains largely unexplored. We recently failed to find any age-independent link between dewlap size and social status in the common eland (Tragelaphus oryx), pointing to the possibility that sexual selection may not be the primary cause of dewlap evolution in ungulates. Here I use a two-pronged approach to test hypotheses on the function of ungulate dewlaps: an interspecific comparative analysis of bovids and deer, and an intraspecific study of eland antelopes in the wild.

Results

Across species, the presence of dewlaps in males was not found to be associated with sexual size dimorphism, a commonly used measure of the intensity of sexual selection. The presence of dewlaps was, however, linked to very large male body size (>400 kg), which agrees with a thermoregulatory function as lower surface/volume-ratio counteracts heat dissipation in large-bodied species. In eland antelopes, large dewlap size was associated with higher, rather than lower, incidence of claw-marks (independently of age), a result which speaks against the dewlap as a predator deterrent and rather indicates a predation cost of the structure.

Conclusion

The findings suggest that, although an additional function in communication should not be ruled out, the dewlap of ungulates may contrast with that of lizards and birds in thermoregulation being a primary function.

     

Lighting environment predicts the relative abundance of male colour morphs in bluefin killifish (Lucania goodei) populations

Animal communication occurs when an animal emits a signal, the signal is transmitted through the environment, and then detected by the receiver. The environment in which signalling occurs should govern the efficacy of this process. In this study, I examine the relationship of lighting environment (light transmission and tree cover), location and the relative abundances of male colour morphs across seven drainages and 30 populations in the bluefin killifish, Lucania goodei. I found that males with blue anal fins were more common in populations with low transmission of ultraviolet (UV) and blue wavelengths. By contrast, males with red anal fins (and to a lesser extent, males with yellow anal fins) were more common in populations with high transmission of UV and blue wavelengths. High UV-blue light transmission should create a blue visual background and may make blue males less conspicuous and red males more conspicuous to conspecifics. Colour contrast with the visual background may be more important than total brightness of the colour pattern. These results indicate that natural selection for effective intraspecific communication drives the relative abundance of male colour morphs in different lighting habitats.     

Sensory response patterns and the evolution of visual signal design in anoline lizards

 The evolutionary relationship between visual system response and visual signal design was investigated in four species of anoline lizards which occupy distinctly different habitats. Anoles display with motion patterns of a colorful throat fan called the dewlap. We assessed signal visibility by recording evoked potentials from the optic tectum in response to a moving stimulus flag (a dewlap-like stimulus), and, in one species, by testing behavioral response. The motion pattern, intensity and spectral quality of the stimulus flag, and the background against which it was viewed, were independently manipulated. In all cases, high-velocity motion patterns with a high percentage of brightness contrast between stimulus and background produced the greatest response. Differences in spectral quality between stimulus and background (color contrast) had no effect on tectal responses, but did influence the behaviorally measured detection probability. Using habitat light data we estimated the visibility of the dewlap of each species in different natural habitats. Each species' dewlap was highly visible in its own habitat, but some were much less visible in the habitats of some other species. Habitat light conditions and visual system response properties appear to have constrained the evolution of dewlap design, in at least some of the species. Accepted: May 1998     

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the ‘laws of inheritance’. Although a number of studies have supported this view by demonstrating substantial between‐sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative‐genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half‐sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance–covariance structure ( G ) that is broadly similar in males ( G _m) and females ( G _f). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between‐sex genetic correlations (r_mf), sexually dimorphic features, such as area and brightness, exhibit reduced r_mf values that do not differ from zero. Using a modified random skewers analysis, we show that the between‐sex genetic variance–covariance matrix ( B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.     

Conspicuous Coloration in Males of the Damselfly Nehalennia irene (Zygoptera: Coenagrionidae): Do Males Signal Their Unprofitability to Other Males?

In damselflies, sexual colour dimorphism is commonly explained as a consequence of selection on traits that increase male attractiveness to females. However, while many species in the damselfly family Coenagrionidae (Insecta: Odonata) are sexually dimorphic, the males do not engage in displays, and male competition for mates resembles a “scramble”. An alternative explanation for the sexual differences in coloration within these species is that sexual dimorphism has evolved as a sex-related warning signal, with males signalling their uprofitability as mates to other males, thereby avoiding harassment from conspecifics. We evaluated an underlying assumption of the theory that male-male harassment rate is influenced by colour by comparing harassment of males of the species Nehalennia irene that had been painted to make them appear: (i) similar to an unaltered male (blue), (ii) different from a male (orange) and (iii) more similar to a female (black). When caged together we found that blue-painted males experienced significantly lower harassment than black-painted males. When unpainted males were caged with each type of painted male we found that blue-painted males and the unpainted males housed in the same cages experienced lower rates of harassment than males housed in cages where some males were painted black, suggesting that a single, reliable signal of unprofitability may benefit the individuals that carry it. While our results do not in themselves demonstrate that sexual colour dimorphism originally evolved as an intra-specific warning signal, they do show that harassment is influenced by coloration, and that such selection could conceivably maintain male coloration as a warning signal.     

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice—red versus orange male back plumage colour—but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.     

CORRELATION BETWEEN ANOLIS LIZARD DEWLAP PHENOTYPE AND ENVIRONMENTAL VARIATION INDICATES ADAPTIVE DIVERGENCE OF A SIGNAL IMPORTANT TO SEXUAL SELECTION AND SPECIES RECOGNITION

Although the importance of signals involved in species recognition and sexual selection to speciation is widely recognized, the processes that underlie signal divergence are still a matter of debate. Several possible processes have been hypothesized, including genetic drift, arbitrary sexual selection, and adaptation to local signaling environments. We use comparative analyses to investigate whether the remarkable geographic variation of dewlap phenotype in a Hispaniolan trunk Anolis lizard (A. distichus) is a result of adaptive signal divergence to heterogeneous environments. We recover a repeated pattern of divergence in A. distichus dewlap color, pattern, and size with environmental variation across Hispaniola. These results are aligned with ecological models of signal divergence and provide strong evidence for dewlap adaptation to local signaling environments. We also find that A. distichus dewlaps vary with the environment in a different manner to other previously studied anoles, thus expanding upon previous predictions on the direction dewlaps will diverge in perceptual color space in response to the environment.     

SEXUAL SELECTION AND THE EVOLUTION OF COMPLEX COLOR PATTERNS IN DRAGON LIZARDS

Many species have elaborate and complex coloration and patterning, which often differ between the sexes. Sexual selection may increase the size or intensity of color patches (elaboration) in one sex or drive the evolution of novel signal elements (innovation). The latter potentially increases color pattern complexity. Color pattern complexity may also be influenced by ecological factors related to predation and environment; however, very few studies have investigated the effects of both sexual and natural selection on color pattern complexity across species. We used a phylogenetic comparative approach to examine these effects in 85 species and subspecies of Australian dragon lizards (family Agamidae). We quantified color pattern complexity by adapting the Shannon–Wiener diversity index. There were clear sex differences in color pattern complexity, which were positively correlated with both sexual dichromatism and sexual size dimorphism, consistent with the idea that sexual selection plays a significant role in the evolution of color pattern complexity. By contrast, we found little evidence of a link between environmental factors and color pattern complexity on body regions exposed to predators. Our results suggest that sexual selection rather than natural selection has led to increased color pattern complexity in males.     

Signal content of red facial coloration in female mandrills (Mandrillus sphinx)

Studies of secondary sexual ornamentation and its maintenance by sexual selection tend to focus on males; however, females may also possess showy ornaments. For example, female mandrills possess facial coloration that ranges from black to bright pink. We used fortnightly photographs of 52 semi-free-ranging females aged above 3years over 19 months to evaluate whether colour conveys information concerning female competitive ability, reproductive quality, age or reproductive status. Colour was not related to female rank or quality (body mass index, age at first birth or mean inter-birth interval); however, colour did increase significantly with age and primiparous females were darker than multiparous females. Colour may therefore signal reproductive quality, as younger females are less fertile and produce smaller offspring. Colour was brighter during the follicular phase than during the luteal phase, suggesting that it may signal fertility. Colour also varied across gestation and peaked at four and eight weeks post-parturition, suggesting that it may signal approaching parturition and lactation. Future studies should examine the relationship between colour and the menstrual cycle in more detail, the hormonal basis of female colour, and determine experimentally whether mandrills of both sexes attend to differences in colour between and within females.     

Extra-pair paternity and sexual dimorphism in birds

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.     

Habitat light and dewlap color diversity in four species of Puerto Rican anoline lizards

Closely related species often have signals that differ dramatically in design. The evolution of such differences may be important in the process of speciation. Selection for signal detectability under different habitat conditions has been proposed as a mechanism leading to the evolution of signal diversity. We examined dewlap color in four closely related species of Anolis lizards that occupy habitats with different light conditions. Initially, we tested the hypothesis that lizards choose specific light conditions within each habitat in which to signal. We rejected this hypothesis for all four species. We next calculated the detectability of the dewlap color of all four species at display locations in each habitat. If selection for detectability under the different light conditions explained the divergence in signal design, the occupant of a given habitat was predicted to have the highest signal detectability in that habitat. However, the rank order of detectability of the four dewlap colors was nearly the same in all four habitats. We concluded that divergent selection for signal detectability does not, by itself, explain the evolution of dewlap color diversity. We hypothesize that the evolution of dewlap color diversity results from simultaneous selection for multiple functions of dewlap color.     

Sexual selection as a promoter of population divergence in male phenotypic characters: a study on mainland and islet lizard populations

Sexual selection is often viewed as a promoter of population divergence, although some forms of sexual selection could rather hamper divergence. In the present study, we investigated whether sexual selection promotes divergence in sexually‐selected traits. We studied population variation in sexual selection in relation to colour morph and body size in islet and mainland populations of the Skyros wall lizard (Podarcis gaigeae). Females were most likely to mate with orange‐throated males with small body sizes, and male body size and coloration were therefore subject to correlational sexual selection. By contrast, male mating probabilities were not affected by any female phenotypic character. We also found variation in a female resistance trait (escape propensity), with females being more prone to escape when exposed to males from other habitats. Sexual selection could potentially affect the frequencies of throat colour morphs in this species by favouring orange‐throated males of small body size, although there was no evidence of sexual selection for local mates or rare phenotypes. The results obtained in the present study thus do not support a role for sexual selection as a promoter of population divergence in this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 374–389.     

Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity

Sexual dichromatism, a form of sexual dimorphism in which males and females differ in colour, is widespread in animals but has been predominantly studied in birds, fishes and butterflies. Moreover, although there are several proposed evolutionary mechanisms for sexual dichromatism in vertebrates, few studies have examined this phenomenon outside the context of sexual selection. Here, we describe unexpectedly high diversity of sexual dichromatism in frogs and create a comparative framework to guide future analyses of the evolution of these sexual colour differences. We review what is known about evolution of colour dimorphism in frogs, highlight alternative mechanisms that may contribute to the evolution of sexual colour differences, and compare them to mechanisms active in other major groups of vertebrates. In frogs, sexual dichromatism can be dynamic (temporary colour change in males) or ontogenetic (permanent colour change in males or females). The degree and the duration of sexual colour differences vary greatly across lineages, and we do not detect phylogenetic signal in the distribution of this trait, therefore frogs provide an opportunity to investigate the roles of natural and sexual selection across multiple independent derivations of sexual dichromatism.     

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.     

Elevational plumage divergence in the Rufous-capped Babbler (Cyanoderma ruficeps) on a mountainous island

Environment plays an important role in the evolution of plumage coloration in birds and may also lead to sexual dichromatism if males and females face different selection pressures. Mountains exhibit varying ecological conditions along their elevation gradient that may impose divergent selection on elevationally widespread species, causing intraspecific plumage divergence. For example, UV light environments often vary between montane and lowland habitats, which could potentially cause differences in plumage UV reflection between birds occurring in the two types of habitats. However, few studies have examined the effects of elevation on plumage evolution. In this study, we quantified the plumage coloration of the Rufous-capped Babbler Cyanoderma ruficeps from montane and lowland habitats on a mountainous island, Taiwan. We aimed to examine whether their plumage showed differences associated with changing ecological environments across the elevational gradient. The results supported that the plumage of babblers occupying montane habitats had higher UV-reflectance and brightness than that of lowland birds, corresponding to the higher UV intensity in montane than lowland background light environments. The elevational differences were mainly found across the ventral parts of babblers that had relatively higher levels of UV reflectance compared with their dorsal parts. Alternatively, the brighter plumage, with higher UV-reflectance in montane than lowland birds, might be mediated by physiological adaptation to other ecological factors, such as parasite pressures. The elevational differences in plumage UV-reflectance and brightness were more dramatic in males than in females. However, we found significant sexual dichromatism in different body parts between montane and lowland babblers in which females had brighter or stronger UV-associated coloration than males, suggesting that sexual selection has little impact on babbler plumage. Our study suggests the importance of elevational divergent selection associated with UV light or other ecological environments on avian plumage evolution.     

Sexual dimorphism in conspicuousness and ornamentation in the enigmatic leaf‐nosed lizard Ceratophora tennentii from Sri Lanka

Measures of physiological performance capacity, such as bite force, form the functional basis of sexual selection. Information about fighting ability may be conveyed through a structural feature such as a rostrum (i.e. horn) or a colour signal and thereby help reduce costly conflict. We quantified sexual dimorphism in key traits likely to be the targets of sexual selection in Tennent's leaf‐nosed lizard (Ceratophora tennentii) from Sri Lanka, and examined their relationship to bite force and body condition. We found body length and bite force to be similar for males and females. However, head length was significantly greater in males and they had significantly more conspicuous throats and labials (chromatic contrast and luminance) than females. Males also had a proportionally larger rostrum, which we predicted could be an important source of information about male quality for both sexes. Rostrum length was correlated with throat chromatic contrast in males but not females. Nonetheless, the rostrum and aspects of coloration did not correlate with bite force or body condition as we predicted. We have no information on contest escalation in this species but if they rarely bite, as suggested by a lack of difference in bite force between males and females, then bite force and any associated signals would not be a target of selection. Finally, males and females had similar spectral reflectance of the mouth and tongue and both had a peak in the ultra‐violet, and were conspicuous to birds. Lizards only gaped their mouths during capture and not when threatened by a potential predator (hand waving). We hypothesize that conspicuous mouth colour may act as a deimatic signal, startling a potential predator, although this will need careful experimental testing in the future.