Physiological basis of convergent evolution in animal communication systems.

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, which 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.

Acute hypoxia exposure rapidly triggers behavioral changes linked to cutaneous gas exchange in Lake Titicaca frogs.

Ventilation is critical to animal life-it ensures that individuals move air/water across their respiratory surface, and thus it sustains gas exchange with the environment. Many species have evolved highly specialized (if not unusual) ventilatory mechanisms, including the use of behavior to facilitate different aspects of breathing. However, these behavioral traits are often only described anecdotally, and the ecological conditions that elicit them are typically unclear. We study one such "ventilation behavior" in Lake Titicaca frogs (Telmatobius culeus). These frogs inhabit high-altitude (i.e., low oxygen) lakes in the Andean Mountains of South America, and they have become textbook examples of cutaneous gas exchange, which is essentially breathing that occurs across the skin. Accordingly, this species has evolved large, baggy skin-folds that dangle from the body to increase the surface area for ventilation. We show that individuals exposed to acute hypoxic conditions that mirror what free-living individuals likely encounter quickly (within minutes) decrease their activity levels, and thus become very still. If oxygen levels continue to decline, the frogs soon begin to perform push-up behaviors that presumably break the low-oxygen boundary layer around skin-folds to increase the conductance of the water/skin gas exchange pathway. Altogether, we suspect that individuals rapidly adjust aspects of their behavior in response to seemingly sudden changes to the oxygen environment as a mechanism to fine tune cutaneous respiration.

Comment on 'Parasite defensive limb movements enhance acoustic signal attraction in male little torrent frogs'.

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.

Activational vs. organizational effects of sex steroids and their role in the evolution of reproductive behavior: Looking to foot-flagging frogs and beyond.

Sex steroids play an important role in regulation of the vertebrate reproductive phenotype. This is because sex steroids not only activate sexual behaviors that mediate copulation, courtship, and aggression, but they also help guide the development of neural and muscular systems that underlie these traits. Many biologists have therefore described the effects of sex steroid action on reproductive behavior as both "activational" and "organizational," respectively. Here, we focus on these phenomena from an evolutionary standpoint, highlighting that we know relatively little about the way that organizational effects evolve in the natural world to support the adaptation and diversification of reproductive behavior. We first review the evidence that such effects do in fact evolve to mediate the evolution of sexual behavior. We then introduce an emerging animal model - the foot-flagging frog, Staurois parvus - that will be useful to study how sex hormones shape neuromotor development necessary for sexual displays. The foot flag is nothing more than a waving display that males use to compete for access to female mates, and thus the neural circuits that control its production are likely laid down when limb control systems arise during the developmental transition from tadpole to frog. We provide data that highlights how sex steroids might organize foot-flagging behavior through its putative underlying mechanisms. Overall, we anticipate that future studies of foot-flagging frogs will open a powerful window from which to see how sex steroids influence the neuromotor systems to help germinate circuits that drive signaling behavior. In this way, our aim is to bring attention to the important frontier of endocrinological regulation of evolutionary developmental biology (endo-evo-devo) and its relationship to behavior.

Testosterone amplifies the negative valence of an agonistic gestural display by exploiting receiver perceptual bias.

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.

A Common Endocrine Signature Marks the Convergent Evolution of an Elaborate Dance Display in Frogs.

AbstractUnrelated species often evolve similar phenotypic solutions to the same environmental problem, a phenomenon known as convergent evolution. But how do these common traits arise? We address this question from a physiological perspective by assessing how convergence of an elaborate gestural display in frogs (foot-flagging) is linked to changes in the androgenic hormone systems that underlie it. We show that the emergence of this rare display in unrelated anuran taxa is marked by a robust increase in the expression of androgen receptor (AR) messenger RNA in the musculature that actuates leg and foot movements, but we find no evidence of changes in the abundance of AR expression in these frogs' central nervous systems. Meanwhile, the magnitude of the evolutionary change in muscular AR and its association with the origin of foot-flagging differ among clades, suggesting that these variables evolve together in a mosaic fashion. Finally, while gestural displays do differ between species, variation in the complexity of a foot-flagging routine does not predict differences in muscular AR. Altogether, these findings suggest that androgen-muscle interactions provide a conduit for convergence in sexual display behavior, potentially providing a path of least resistance for the evolution of motor performance.