Mechanosensory Signaling in Axolotl Courtship and Evolution of Communication

In behavioral biology, many models have been proposed to explain how communication systems evolve. Within neuroethology, the principle of sender-receiver matching has spurred much research in auditory communication, but fewer studies on mechanosensory communication. We investigated sender-receiving matching in mechanosensory communication, focusing on the "hula", a courtship behavior that produces an undulating movement of the tail, in axolotls (Ambystoma mexicanum), an aquatic salamander. We characterized typical courtship behaviors, then quantified tail-motion parameters (speed, sweep angle, and elevation angle) from males as they performed the hula. We then constructed a "Robotail", a robotic device that mimics the physical and motion properties of the male tail during courtship. Interestingly, females initially responded to the Robotail as if it were a prey item, an effect that was mitigated by the addition of male whole-body odorants. We examined female behavioral responses to changes in individual Robotail movement parameters and found that speed and sweep angle were important to locomotion. Females transitioned between locomotor states more often when exposed to combinations of wide sweep angles and fast speeds from the Robotail, which males perform moderately or rarely, perhaps reflecting a preference for vigorous movements. We then assessed neural responses to stimuli generated by the Robotail by recording from the anterodorsal lateral line nerve (ADLLn), which innervates the mechanosensory neuromasts on the snout. The female ADLLn responded most vigorously when stimulated with moderate sweep angles and speeds, parameters often used by courting males. Thus, our behavioral results support a receiver bias model but our neurophysiological results support a sender-receiver matching model within mechanosensory communication during courtship in axolotls. Our results also provide novel evidence that mechanosensory cues generated during hula behavior in salamanders play a role in courtship.