Sex steroids affect the motivation to court mates, but less is known about how they influence motor movements associated with courtship behavior. Steroidal control of motor function may be especially important for species in which courtship requires superior strength, stamina, and neuromuscular coordination. Here we use the golden-collared manakin (Manacus vitellinus) to examine whether the neuromuscular circuitry that controls motoric aspects of courtship activity is sensitive to androgens. Males of this tropical species attract mates by rapidly jumping among branches in a courtship arena and using their wings to produce loud wing snaps. Testosterone activates this display via the androgen receptor (AR), and past work reveals that manakins injected with radio-labeled T ((3)H-T) accumulate radioactivity in the spinal cord. Thus, we used quantitative PCR to measure AR, estrogen receptor-α (ER-α) subtype, and aromatase (AROM) mRNA in spinal cords of male and female manakins and zebra finches. Expression of AR, but not ER-α or aromatase, was higher throughout the manakin spinal cord compared with the zebra finch. Next, we tested whether AR-expressing skeletal muscles are innervated by motor and sensory neurons that also express AR. To do this, we backfilled spinal neurons by injecting fluorescent tracers into select AR-sensitive wing and leg muscles of wild caught male and female manakins. We then removed these spinal cords and measured AR expression with in situ hybridization. Both sexes showed abundant AR mRNA in the cervical and lumbosacral spinal enlargements as well as in dorsal root ganglia attached to these enlargements. Together our findings suggest that androgens act widely on peripheral motor and sensory circuits in golden-collared manakins to influence wing snapping displays.
Elaborate courtship displays are relatively common features of the masculine reproductive behavior in birds. However, little is known about their neural and hormonal control. One bird that performs such a display is the golden-collared manakin (Manacus vitellinus) of Panamanian forests. Adult males, but not females, perform a physically intense display requiring substantial neuromuscular control of the wings and legs. We tested the hypothesis that steroid sensitivity is a property of neurons in the manakin spinal cord. Males and females were captured from active courtship leks, treated with drugs to block steroidogenesis, injected with 3 H-labeled testosterone, and the spinal cords were removed and processed for autoradiography. Sex steroid-accumulating cells were widely distributed in the spinal cords in each of six males and in one of five females. Cells, including presumptive motoneurons, reached their highest density in the ventral horns of the cervical and lumbosacral enlargements, regions associated with motor control of the wings and legs. These results suggest that neurons in the adult manakin spinal cord can express sex-steroid receptors, but do so less in females than in males. This evidence for androgen sensitivity and sexual dimorphism in the adult avian spinal cord suggests that sex steroids may control diverse behaviors in male birds in part by acting directly on the spinal neural circuits.
In oscine passerines, the telencephalon expresses high levels of the estrogen synthetic enzyme aromatase. In contrast, forebrain aromatase is limited to low levels at discrete limbic loci in non-passerines. The function of forebrain aromatase in oscines is unknown, however, estrogen-sensitive elements of the telencephalic song circuit (an oscine characteristic) may be influenced by local aromatization. Very few studies have investigated the neuroendocrine characteristics of sub-oscine passerines. Species of this passerine sub-order are taxonomically similar to oscines, but do not appear to learn how to sing as oscines, and show no evidence of a song circuit. The neural expression of aromatase in these birds is unknown. We asked whether the golden-collared manakin, a sub-oscine, (a) showed evidence of a song circuit, and (b) expressed aromatase in the telencephalon at high levels like the zebra finch (oscine passerine) or at low levels like the quail (non-passerine). Nissl stains and immunocytochemistry for microtubule associated proteins showed no evidence of a song circuit in manakins of either sex, whereas both techniques delineate all song nuclei in the zebra finch. However, biochemical and immunocytochemical measures reveal that in the manakin, several telencephalic loci, including the hippocampus, caudomedial neostriatum, nucleus taeniae, and the lateral neostriatum express aromatase. Assays run in parallel show low to undetectable levels of aromatase in the telencephalon of the quail (nonpasserine) and abundant levels in the zebra finch (oscine passerine), suggesting a dissociation between the presence of a song circuit and forebrain aromatase expression in this sub-oscine. These data suggest that forebrain aromatase may have evolved in sub-oscine songbirds before the evolution of a song circuit and singing behavior in oscines. Alternatively, forebrain aromatase may serve functions distinct from singing behavior.
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