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Synopsis To humans, the diverse array of display behaviors that animals use for communication can easily seem peculiar or bizarre. While ample research delves into the evolutionary principles that shape these signals’ effectiveness, little attention is paid to evolutionary patterning of signal design across taxa, particularly when it comes to the potential convergent evolution of many elaborate behavioral displays. By taking a mechanistic perspective, we explore the physiological and neurobiological mechanisms that likely influence the evolution of communication signals, emphasizing the utilization of pre-existing structures over novel adaptations. Central to this investigation are the concepts of perceptual bias and ritualization that we propose contribute to the convergence of elaborate display designs across species. Perceptual bias explains a phenomenon where pre-existing perceptual systems of receivers, used for innate behaviors such as food and predator recognition, select for certain traits of a communication signal from a signaler. Ritualization occurs when traits with no functional role in communication are co-opted through selection and transformed into a new communicative signal. Importantly, susceptibility for ritualization can be brought about through physiological modifications that occurred early in evolutionary time. In this way, perceptual bias can be a selective force that causes the co-option of non-communicative traits into a new communication signal through ritualization involving pre-existing modifications to physiological systems. If the perceptual bias, non-communicative signal, and physiological modifications that increase susceptibility to ritualization are highly conserved, then we may see the convergent evolution of the new communication signal with unrelated taxa facing similar sensory constraints. We explore this idea here using the foot-flagging frog system as a theoretical case study. 

Zhao et al. recently reported results which, they claim, suggest that sexual selection produces the multimodal displays seen in little torrent frogs (Amolops torrentis) by co-opting limb movements that originally evolved to support parasite defense (Zhao et al., 2022). Here, we explain why we believe this conclusion to be premature. 

AbstractA diversity of defence colourations that shift over time provides protection against natural enemies. Adaptations for camouflage depend on an organism’s interactions with the natural environment (predators, habitat), which can change ontogenetically. Wallace’s flying frogs (Rhacophorus nigropalmatus) are cryptic emerald green in their adult life stage, but juveniles are bright red and develop white spots on their back 1 month after metamorphosis. This latter conspicuous visual appearance might function as antipredator strategy, where frogs masquerade as bird or bat droppings so that predators misidentified them as inedible objects. To test this idea, we created different paraffin wax frog models—red with white spots, red without white spots, green, and unpainted—and placed them in equal numbers within a > 800 m²rainforest house at the Vienna Zoo. This environment closely resembles the Bornean rainforest and includes several free-living avian predators of frogs. We observed an overall hit rate of 15.5%. A visual model showed that the contrast of red, green and control models against the background colouration could be discriminated by avian predators, whereas green models had less chromatic difference than red morphs. The attack rate was significantly greater for red but was reduced by half when red models had white spots. The data therefore supports the hypothesis that the juvenile colouration likely acts as a masquerade strategy, disguising frogs as animal droppings which provides similar protection as the cryptic green adult colour. We discuss the ontogenetic colour change as a possible antipredator strategy in relation to the different habitats used at different life stages. Significance statementPredation pressure and the evolution of antipredator strategies site at the cornerstone of animal-behaviour research. Effective antipredator strategies can change in response to different habitats that animals use during different life stages. We study ontogenetic shifts in colour change as dynamic antipredator strategy in juvenile and adult Wallace’s flying frogs. We show that the unusual colour pattern of juveniles (bright red with small white spots) likely functions as a masquerade of animal droppings. Specifically, we show that white dotting, which can be associated with animal faeces, acts as the main visual feature that turns an otherwise highly conspicuous individual into a surprisingly camouflaged one. To our knowledge, this is the first experimental exploration of a vertebrate masquerading as animal droppings. 

Many animals communicate by rapidly (within minutes or seconds) changing their body coloration; however, we know little about the physiology of this behaviour. Here we study how catecholaminergic hormones regulate rapid colour change in explosive breeding toads ( Duttaphrynus melanostictus ), where large groups of males gather and quickly change their colour from brown to bright yellow during reproduction. We find that both epinephrine (EP) and/or norepinephrine (NE) cause the toads' skin to become yellow in minutes, even in the absence of social and environmental cues associated with explosive breeding. We hypothesize that natural selection drives the evolution of rapid colour change by co-opting the functional effects of catecholaminergic action. If so, then hormones involved in ‘fight or flight’ responses may mechanistically facilitate the emergence of dynamic visual signals that mediate communication in a sexual context. 

Many animals communicate by performing elaborate displays that are incredibly extravagant and wildly bizarre. So, how do these displays evolve? One idea is that innate sensory biases arbitrarily favour the emergence of certain display traits over others, leading to the design of an unusual display. Here, we study how physiological factors associated with signal production influence this process, a topic that has received almost no attention. We focus on a tropical frog, whose males compete for access to females by performing an elaborate waving display. Our results show that sex hormones like testosterone regulate specific display gestures that exploit a highly conserved perceptual system, evolved originally to detect ‘dangerous' stimuli in the environment. Accordingly, testosterone makes certain gestures likely to appear more perilous to rivals during combat. This suggests that hormone action can interact with effects of sensory bias to create an evolutionary optimum that guides how display exaggeration unfolds.