Hormones and the neuromuscular control of courtship in the golden-collared manakin (Manacus vitellinus)

Abstract

Many animals engage in spectacular courtship displays, likely recruiting specialized neural, hormonal and muscular systems to facilitate these performances. Male golden-collared manakins (Manacus vitellinus) of Panamanian rainforests perform physically elaborate courtship displays that include novel forms of visual and acoustic signaling. We study the behavioral neuroendocrinology of this male's courtship, combining field behavioral observations with anatomical, biochemical and molecular laboratory-based studies. Seasonally, male courtship is activated by testosterone with little correspondence between testosterone levels and display intensity. Females prefer males whose displays are exceptionally frequent, fast and accurate. The activation of androgen receptors (AR) is crucial for optimal display performance, with AR expressed at elevated levels in several neuromuscular tissues. Apparently, courtship enlists an elaborate androgen-dependent network that includes spinal motoneurons, skeletal muscles and somatosensory systems. This work highlights the value of studying non-traditional species to illuminate physiological adaptations and, hopefully, stimulates future research on other species with complex behaviors.

Keywords: 5Alpha-reductase; Androgen receptors; Androgens; Aromatase; Behavioral ecology; Estrogens; Neuroendocrinology; Sex steroids; Songbirds; Spinal cord.

Fig. 1

A schematic moving clockwise of the courtship dance of the male golden-collared manakin (Manacus vitellinus) being observed by a female, the solid gray bird perched above the male. The display begins (1) with the male sitting rigid on a upright stem. He launches his body from the perch with a powerful thrust of his legs (2). Midflight, he makes a single powerful and rapid wing stroke (3) that produces the loud single snap. He retracts his wings and holds them in place, sailing across the arena while still holding his “beard” solidly out in front. Just before landing, he makes a quick partial wing flap that turns him in midair and he lands squarely on the second stem (4). He holds this position briefly rigidly until embarking on the next jump and wingsnap. The thick arrow indicates that this complete sequence is repeated, on average, about nine times per complete courtship display. Note that in some cases, the female joins the male in a “duo dance” but she flies, not jumps, across the arena and her movements appear more awkward.

Fig. 2

Schematic illustrating the male golden-collared manakin courtship season in central Panama (green) that peaks between mid-January to mid-June relative to relative mean plasma testosterone levels (orange) and relative monthly rainfall amounts (blue). Note plasma T levels are very variable during the dry-season when courting is at its peak.

Fig. 3

Photomicrographs of androgen receptor (AR) expressing cells in the golden-collared manakin spinal cord. The top panel (a) shows spinal motoneurons that innervate the wing-lifting supracoracoideus (SC) muscle, whereas the bottom panel (b) shows cells in the dorsal root ganglia, which relay somatic information from the SC to the spinal cord. On the left, photomicrographs show cells labeled with fluorescent tracers under ultraviolet illumination. On the right, photomicrographs show the same tissue under dark-field illumination to illustrate hybridization of the AR in situ probe. In the center, photomicrographs show an overlay of the images from the left and right; this image indicates that fluorescent cells express abundant AR mRNA. White arrows point to the same cell in all three images. Reference bar = 40 μm. Figures are modified from (Fuxjager et al., 2012a).

Fig. 4

Expression and function of androgen receptors (AR) in the male golden-collared manakin supracoricoideus (SC) wing muscle. The top figure (a) shows that AR mRNA expression is significantly higher in golden-collared manakin SC than in the SC of either the ochre-bellied flycatcher (a tropical suboscine) or the zebra finch (a classic oscine model). The middle figure (b) shows that activity levels of the 5α-reductase enzyme are greater in the golden-collared manakin SC as compared to the zebra finch SC. As such, the manakin SC has a greater capacity to locally covert testosterone to the more potent 5α-DHT. The bottom graph (c) shows that, in golden-collared manakins, testosterone increases expression of parvalbumin mRNA in the SC. This indicates that muscular AR in this species is functional. All significant differences are denoted by asterisks (*) above the relevant bars, and data represent mean ± 1SEM. Data are taken from (Feng et al., 2010; Fuxjager et al., 2012a).

Fig. 5

Summary schematic of a reproductively active male golden-collared manakin and an androgen sensitive neuromuscular circuit that presumably underlies his remarkable courtship display. The male is perched and is repeatedly snapping his wings together above its head to produce a roll-snap sonations. The thin arrows point to tissues within the manakin on which androgens, like testosterone (T), act to influence wing-snap behavior (by their high expression of androgen-receptors). These tissues include the brain (highlighted in orange), the spinal cord (highlighted in yellow), and the three main muscles that control the wing (highlighted in pink). The largest of the three highlighted muscles is the pectoralis (PEC), which retracts the wing upon contraction. Deep to the PEC, however, is the supracoicoideus (SC), which is depicted by a darker pink and the dashed lines running through the PEC. The SC helps raise the wing when it contracts. The final muscle is the dorsal scapulohumeralis caudalis (SH) that helps stabilize and elevate the wing upon contraction (Dial, 1992; Schultz et al., 2001; Bostwick and Prum, 2003). The thick arrow points to the manakin’s radius (highlighted in green). Preliminary evidence from our laboratory shows that this bone is flattened as compared to other species and thus may facilitate sounds production of wing-snaps.