Vomeronasal organ volume increases with body size and is dissociated with the loss of a visual signal in Sceloporus lizards.

Many organisms communicate using signals in different sensory modalities (multicomponent or multimodal). When one signal or component is lost over evolutionary time, it may be indicative of changes in other characteristics of the signalling system, including the sensory organs used to perceive and process signals. Sceloporus lizards predominantly use chemical and visual signals to communicate, yet some species have lost the ancestral ventral colour patch used in male-male agonistic interactions and exhibit increased chemosensory behaviour. Here, we asked whether evolutionary loss of this sexual signal is associated with larger vomeronasal organ (VNO) volumes (an organ that detects chemical scents) compared with species that have retained the colour patch. We measured VNO coronal section areas of 7-8 adult males from each of 11 Sceloporus species (4 that lost and 7 that retained the colour patch), estimated sensory and total epithelium volume, and compared volumes using phylogenetic analysis of covariance, controlling for body size. Contrary to expectations, we found that species retaining the ventral patch had similar relative VNO volumes as did species that had lost the ancestral patch, and that body size explains VNO epithelium volume. Visual signal loss may be sufficiently compensated for by increased chemosensory behaviour, and the allometric pattern may indicate sensory system trade-offs for large-bodied species.

Oestradiol reduces female bill colour in a mutually ornamented bird.

Carotenoid-based colour signals can be costly to produce and maintain, and trade-offs between signalling and other fitness traits are expected. In mutually ornamented species, trade-offs with reproduction may be stronger for females than males, because females often dedicate more resources to offspring production, which may lead to plastic investment in colour signals and plastic sexual dichromatism. Oestradiol is a candidate mediator of this trade-off because it regulates reproductive physiology and may also influence the expression of coloration. We tested this hypothesis by giving female common waxbills (Estrilda astrild) either oestradiol (17ß-oestradiol) or empty implants during the early breeding season and measured spectral reflectance of carotenoid-based bill coloration weekly for two months. Using a model of avian vision, we found that bill colour in oestradiol-implanted females became less saturated, less red in hue and brighter, compared with control females and with unimplanted males. This resulted in a change in bill sexual dichromatism from imperceptible to perceptible. Results support the hypothesis that female reproductive physiology influences investment in coloration through changes in oestradiol and show a form of female-driven plastic sexual dichromatism. Greater sensitivity of female colour to physiological and/or environmental conditions helps explain why differences in sexual dichromatism among species differing in ecology often evolve owing to changes in female rather than male phenotype.

Information out of the blue: phenotypic correlates of abdominal color patches in Sceloporus lizards.

Colorful ornaments are important visual signals for animal communication that can provide critical information about the quality of the signaler. In this study, we focused on different color characteristics of the abdominal patches of males of six lizard species from the genus Sceloporus. We addressed three main objectives. First, we examined if size, brightness, saturation, and conspicuousness of these ornaments are indicative of body size, condition, immune function, or levels of testosterone and corticosterone. Second, we evaluated if the distinct components of these abdominal patches (blue or green patches and black stripes) transmit similar information about the signaler, which would support the redundant signal hypothesis, or if these components are related to different phenotypic traits, which would support the multiple message hypothesis. Third, we compared the phenotypic correlates of these ornaments among our six species to understand the degree of conservatism in the signaling patterns or to find species-specific signals. Using data collected from males in natural conditions and a multi-model inference framework, we found that in most species the area of the patches and the brightness of the blue component are positively related to body size. Thus, these color characteristics are presumably indicative of the physical strength and competitive ability of males and these shared signals were likely inherited from a common ancestor. In half of the species, males in good body condition also exhibit relatively larger blue and black areas, suggesting that the expression of these ornaments is condition-dependent. Abdominal patches also provide information about immunocompetence of the males as indicated by different correlations between certain color characteristics and ectoparasite load, counts of heterophils, and the heterophil:lymphocyte ratio. Our findings reveal that area and brightness of the abdominal patches signal the size and body condition of males, whereas blue saturation and conspicuousness with respect to the surrounding substrate are indicative of immune condition, thus supporting the multiple message hypothesis. However, some of these correlations were not shared by all species and, hence, point to intriguing species-specific signals.

Brain transcriptomic responses of Yarrow's spiny lizard, Sceloporus jarrovii, to conspecific visual or chemical signals.

Species with multimodal communication integrate information from social cues in different modalities into behavioral responses that are mediated by changes in gene expression in the brain. Differences in patterns of gene expression between signal modalities may shed light on the neuromolecular mechanisms underlying multisensory processing. Here, we use RNA-Seq to analyze brain transcriptome responses to either chemical or visual social signals in a territorial lizard with multimodal communication. Using an intruder challenge paradigm, we exposed 18 wild-caught, adult, male Sceloporus jarrovii to either male conspecific scents (femoral gland secretions placed on a small pebble), the species-specific push-up display (a programmed robotic model), or a control (an unscented pebble). We conducted differential expression analysis with both a de novo S. jarrovii transcriptome assembly and the reference genome of a closely related species, Sceloporus undulatus. Despite some inter-individual variation, we found significant differences in gene expression in the brain across signal modalities and the control in both analyses. The most notable differences occurred between chemical and visual stimulus treatments, closely followed by visual stimulus versus the control. Altered expression profiles could explain documented aggression differences in the immediate behavioral response to conspecific signals from different sensory modalities. Shared differentially expressed genes between visually- or chemically-stimulated males are involved in neural activity and neurodevelopment and several other differentially expressed genes in stimulus-challenged males are involved in conserved signal-transduction pathways associated with the social stress response, aggression and the response to territory intruders across vertebrates.

Evolutionary loss of a signalling colour is linked to increased response to conspecific chemicals.

Behavioural responses to communicative signals combine input from multiple sensory modalities and signal compensation theory predicts that evolutionary shifts in one sensory modality could impact the response to signals in other sensory modalities. Here, we conducted two types of field experiments with 11 species spread across the lizard genus Sceloporus to test the hypothesis that the loss of visual signal elements affects behavioural responses to a chemical signal (conspecific scents) or to a predominantly visual signal (a conspecific lizard), both of which are used in intraspecific communication. We found that three species that have independently lost a visual signal trait, a colourful belly patch, responded to conspecific scents with increased chemosensory behaviour compared to a chemical control, while species with the belly patch did not. However, most species, with and without the belly patch, responded to live conspecifics with increased visual displays of similar magnitude. While aggressive responses to visual stimuli are taxonomically widespread in Sceloporus, our results suggest that increased chemosensory response behaviour is linked to colour patch loss. Thus, interactions across sensory modalities could constrain the evolution of complex signalling phenotypes, thereby influencing signal diversity.

Structural Identification, Synthesis and Biological Activity of Two Volatile Cyclic Dipeptides in a Terrestrial Vertebrate.

Single substances within complex vertebrate chemical signals could be physiologically or behaviourally active. However, the vast diversity in chemical structure, physical properties and molecular size of semiochemicals makes identifying pheromonally active compounds no easy task. Here, we identified two volatile cyclic dipeptides, cyclo(L-Leu-L-Pro) and cyclo(L-Pro-L-Pro), from the complex mixture of a chemical signal in terrestrial vertebrates (lizard genus Sceloporus), synthesised one of them and investigated their biological activity in male intra-specific communication. In a series of behavioural trials, lizards performed more chemosensory behaviour (tongue flicks, lip smacks and substrate lickings) when presented with the synthesised cyclo(L-Pro-L-Pro) chemical blend, compared to the controls, the cyclo(L-Leu-L-Pro) blend, or a combined blend with both cyclic dipeptides. The results suggest a potential semiochemical role of cyclo(L-Pro-L-Pro) and a modulating effect of cyclo(L-Leu-L-Pro) that may depend on the relative concentration of both compounds in the chemical signal. In addition, our results stress how minor compounds in complex mixtures can produce a meaningful behavioural response, how small differences in structural design are crucial for biological activity, and highlight the need for more studies to determine the complete functional landscape of biologically relevant compounds.

Corticosterone mediated mate choice affects female mating reluctance and reproductive success.

The study of stress-related hormones as mediators of sexual selection has traditionally focused on the effect of glucocorticoids on male quality and competing ability. However, environmental stressors are expected to affect both males and females, and the strength of sexual selection might be affected by changes in female mating decisions, a hypothesis that has rarely been tested. Here, we investigated whether female common lizard (Zootoca vivipara) mating behaviour and mating preferences are affected by different levels of administered corticosterone and conditioned by the familiarity of their partners, which is known to influence Z. vivipara social behaviour. To this end, two females, one corticosterone-treated and one control female, were simultaneously presented with an unfamiliar male and the following day with either a familiar or an unfamiliar male. Females treated with corticosterone (Cort) were more aggressive towards males and mated less. Furthermore, copulation probability in Cort females, but not in control females, increased with body size. On the second day, Cort females only mated with familiar partners. In contrast, male behaviour towards females was not affected by treatment and only bigger males successfully copulated with Cort females. This shows that corticosterone directly affected female mating behaviour and mating preferences, while male mating behaviour was unaffected by the female's level of corticosterone. Environmental and social stressors may affect reproductive strategies of females, the strength of sexual selection, and sexual conflict through their effects on female glucocorticoid levels, potentially in a wide range of species.

Losing the trait without losing the signal: Evolutionary shifts in communicative colour signalling.

Colour signalling traits are often lost over evolutionary time, perhaps because they increase vulnerability to visual predators or lose relevance in terms of sexual selection. Here, we used spectrometric and phylogenetic comparative analyses to ask whether four independent losses of a sexually selected blue patch are spectrally similar, and whether these losses equate to a decrease in conspicuousness or to loss of a signal. We found that patches were lost in two distinct ways: either increasing reflectance primarily at very long or at very short wavelengths, and that species with additional colour elements (UV, green and pink) may be evolutionary intermediates. In addition, we found that patch spectral profiles of all species were closely aligned with visual receptors in the receiver's retina. We found that loss of the blue patch makes males less conspicuous in terms of chromatic conspicuousness, but more conspicuous in terms of achromatic contrast, and that sexual dimorphism often persists regardless of patch loss. Dorsal surfaces were considerably more cryptic than were ventral surfaces, and species in which male bellies were the most similar in conspicuousness to their dorsal surfaces were also the most sexually dimorphic. These results emphasize the consistent importance of sexual selection and its flexible impact on different signal components through evolutionary time.

Climate Effects on Growth, Body Condition, and Survival Depend on the Genetic Characteristics of the Population.

Climatic change is expected to affect individual life histories and population dynamics, potentially increasing vulnerability to extinction. The importance of genetic diversity has been highlighted for adaptation and population persistence. However, whether responses of life-history traits to a given environmental condition depend on the genetic characteristics of a population remains elusive. Here we tested this hypothesis in the lizard Zootoca vivipara by simultaneously manipulating habitat humidity, a major climatic predictor of Zootoca's distribution, and adult male color morph frequency, a trait with genome-wide linkage. Interactive effects of humidity and morph frequency had immediate effects on growth and body condition of juveniles and yearlings, as well as on adult survival, and delayed effects on offspring size. In yearlings, higher humidity led to larger female body size and lower humidity led to higher male compared to female survival. In juveniles and yearlings, some treatment effects were compensated over time. The results show that individual responses to environmental conditions depend on the population's color morph frequency, age class, and sex and that these affect intra- and inter-age class competition. Moreover, humidity affected the competitive environment rather than imposing trait-based selection on specific color morphs. This indicates that species' responses to changing environments (e.g., to climate change) are highly complex and difficult to accurately reconstruct and predict without information on the genetic characteristics and demographic structure of populations.

Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major).

Carotenoid-based yellowish to red plumage colors are widespread visual signals used in sexual and social communication. To understand their ultimate signaling functions, it is important to identify the proximate mechanism promoting variation in coloration. Carotenoid-based colors combine structural and pigmentary components, but the importance of the contribution of structural components to variation in pigment-based colors (i.e., carotenoid-based colors) has been undervalued. In a field experiment with great tits (Parus major), we combined a brood size manipulation with a simultaneous carotenoid supplementation in order to disentangle the effects of carotenoid availability and early growth condition on different components of the yellow breast feathers. By defining independent measures of feather carotenoid content (absolute carotenoid chroma) and background structure (background reflectance), we demonstrate that environmental factors experienced during the nestling period, namely, early growth conditions and carotenoid availability, contribute independently to variation in yellow plumage coloration. While early growth conditions affected the background reflectance of the plumage, the availability of carotenoids affected the absolute carotenoid chroma, the peak of maximum ultraviolet reflectance, and the overall shape, that is, chromatic information of the reflectance curves. These findings demonstrate that environment-induced variation in background structure contributes significantly to intraspecific variation in yellow carotenoid-based plumage coloration.