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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.

 

Synopsis Lizards use chemical communication to mediate many reproductive, competitive, and social behaviors, but the neuroendocrine mechanisms underlying chemical communication in lizards are not well understood and understudied. By implementing a neuroendocrine approach to the study of chemical communication in reptiles, we can address a major gap in our knowledge of the evolutionary mechanisms shaping chemical communication in vertebrates. The neuropeptide arginine vasotocin (AVT) and its mammalian homolog vasopressin are responsible for a broad spectrum of diversity in competitive and reproductive strategies in many vertebrates, mediating social behavior through the chemosensory modality. In this review, we posit that, though limited, the available data on AVT-mediated chemical communication in lizards reveal intriguing patterns that suggest AVT plays a more prominent role in lizard chemosensory behavior than previously appreciated. We argue that these results warrant more research into the mechanisms used by AVT to modify the performance of chemosensory behavior and responses to conspecific chemical signals. We first provide a broad overview of the known social functions of chemical signals in lizards, the glandular sources of chemical signal production in lizards (e.g., epidermal secretory glands), and the chemosensory detection methods and mechanisms used by lizards. Then, we review the locations of vasotocinergic populations and neuronal projections in lizard brains, as well as sites of peripheral receptors for AVT in lizards. Finally, we end with a case study in green anoles (Anolis carolinensis), discussing findings from recently published work on the impact of AVT in adult males on chemosensory communication during social interactions, adding new data from a similar study in which we tested the impact of AVT on chemosensory behavior of adult females. We offer concluding remarks on addressing several fundamental questions regarding the role of AVT in chemosensory communication and social behavior in lizards. 

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 genusSceloporus), 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.