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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.

SUBMITTER: Mangiamele LA

PROVIDER: S-EPMC4878525 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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

Mangiamele Lisa A LA Fuxjager Matthew J MJ Schuppe Eric R ER Taylor Rebecca S RS Hödl Walter W Preininger Doris D

Proceedings of the National Academy of Sciences of the United States of America 20160503 20

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 ...[more]

PMID: 27143723

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Project description:BackgroundThe shape of the appendicular bones in mammals usually reflects adaptations towards different locomotor abilities. However, other aspects such as body size and phylogeny also play an important role in shaping bone design.We used 3D landmark-based geometric morphometrics to analyse the shape of the hind limb bones (i.e., femur, tibia, and pelvic girdle bones) of living and extinct terrestrial carnivorans (Mammalia, Carnivora) to quantitatively investigate the influence of body size, phylogeny, and locomotor behaviour in shaping the morphology of these bones. We also investigated the main patterns of morphological variation within a phylogenetic context.ResultsSize and phylogeny strongly influence the shape of the hind limb bones. In contrast, adaptations towards different modes of locomotion seem to have little influence. Principal Components Analysis and the study of phylomorphospaces suggest that the main source of variation in bone shape is a gradient of slenderness-robustness.ConclusionThe shape of the hind limb bones is strongly influenced by body size and phylogeny, but not to a similar degree by locomotor behaviour. The slender-robust "morphological bipolarity" found in bone shape variability is probably related to a trade-off between maintaining energetic efficiency and withstanding resistance to stresses. The balance involved in this trade-off impedes the evolution of high phenotypic variability. In fact, both morphological extremes (slender/robust) are adaptive in different selective contexts and lead to a convergence in shape among taxa with extremely different ecologies but with similar biomechanical demands. Strikingly, this "one-to-many mapping" pattern of evolution between morphology and ecology in hind limb bones is in complete contrast to the "many-to-one mapping" pattern found in the evolution of carnivoran skull shape. The results suggest that there are more constraints in the evolution of the shape of the appendicular skeleton than in that of skull shape because of the strong biomechanical constraints imposed by terrestrial locomotion.

Dataset Information

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

Publications

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

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