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

Abstract

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.androgen receptor | testosterone | courtship behavior | signal evolution | frogs

Sex differences in neuromuscular androgen receptor expression and sociosexual behavior in a sex changing fish

“…Therefore, we suggest that differences in androgen sensitivity modulate the ability to produce courtship and agonistic displays more frequently. This idea is supported by research that demonstrates muscles that coordinate sociosexual behaviors, including both courtship and agonistic displays, frequently exhibit increased AR expression [16]. Such elevated androgenic sensitivity likely enhances motor ability by regulating molecular factors that regulate contraction speed and stamina [14, 42–44].…”

Woodpecker drumming behavior is linked to the elevated expression of genes that encode calcium handling proteins in the neck musculature

“…We used quantitative real-time PCR (qPCR) to measure gene expression on an Applied Biosystems 7500 Fast RealTime sequence detection system (Foster City, CA, USA), as described previously (Fuxjager et al, 2012;Mangiamele et al, 2016). In this case, we generated species-specific primers for PV, SERCA1 and RYR1 (Table S2).…”

Skeletal muscles that actuate sexual displays are specialized forde novoandrogen synthesis

“…Here we explore these topics by assessing mechanisms of de novo androgen synthesis in skeletal muscles that support elaborate socio-sexual behavior. Skeletal muscle is a major androgen target in the vertebrate body [11-13], and prior work shows that androgenic regulation of muscle is often necessary for reproduction [14-16]. Courtship is a prime example: muscles that mediate displays used to attract mates are often enriched with androgen receptor [13, 17, 18], and blocking androgenic activation of these receptors disrupts the effectiveness or recognizability of signaling behavior [14-16].…”

“…Skeletal muscle is a major androgen target in the vertebrate body [11-13], and prior work shows that androgenic regulation of muscle is often necessary for reproduction [14-16]. Courtship is a prime example: muscles that mediate displays used to attract mates are often enriched with androgen receptor [13, 17, 18], and blocking androgenic activation of these receptors disrupts the effectiveness or recognizability of signaling behavior [14-16]. Importantly, however, we know that individuals can often produce these same displays when their gonads are not making steroids [4, 5, 19].…”