Increased androgenic sensitivity in the hind limb muscular system marks the evolution of a derived gestural display

Significance Diverse species signal using limb gestures, but little is known about how selection incorporates such movements into display routines. We study this issue in a tropical frog that produces complex waving displays with its hind limbs. We find not only that androgenic hormones activate such signaling behavior, but also that the signal’s recent evolution is marked by a dramatic increase in androgenic sensitivity of the thigh muscles that control hind limb maneuvering. Moreover, we demonstrate that this muscular phenotype mirrors that which is found in the larynx of other frogs that primarily produce androgen-dependent vocalizations as social signals. We therefore uncover strong coevolution between the emergence of complex sexual gestural signals and enhanced androgenic signaling mechanisms in the muscular system. Physical gestures are prominent features of many species’ multimodal displays, yet how evolution incorporates body and leg movements into animal signaling repertoires is unclear. Androgenic hormones modulate the production of reproductive signals and sexual motor skills in many vertebrates; therefore, one possibility is that selection for physical signals drives the evolution of androgenic sensitivity in select neuromotor pathways. We examined this issue in the Bornean rock frog (Staurois parvus, family: Ranidae). Males court females and compete with rivals by performing both vocalizations and hind limb gestural signals, called “foot flags.” Foot flagging is a derived display that emerged in the ranids after vocal signaling. Here, we show that administration of testosterone (T) increases foot flagging behavior under seminatural conditions. Moreover, using quantitative PCR, we also find that adult male S. parvus maintain a unique androgenic phenotype, in which androgen receptor (AR) in the hind limb musculature is expressed at levels ∼10× greater than in two other anuran species, which do not produce foot flags (Rana pipiens and Xenopus laevis). Finally, because males of all three of these species solicit mates with calls, we accordingly detect no differences in AR expression in the vocal apparatus (larynx) among taxa. The results show that foot flagging is an androgen-dependent gestural signal, and its emergence is associated with increased androgenic sensitivity within the hind limb musculature. Selection for this novel gestural signal may therefore drive the evolution of increased AR expression in key muscles that control signal production to support adaptive motor performance.