To hum or not to hum: Neural transcriptome signature of courtship vocalization in a teleost fish

For many animal species, vocal communication is a critical social behavior, often a necessary component of reproductive success. In addition to the role of vocal behavior in social interactions, vocalizations are often demanding motor acts. Through understanding the genes involved in regulating and permitting vertebrate vocalization, we can better understand the mechanisms regulating vocal and, more broadly, motor behaviors. Here, we use RNA-sequencing to investigate neural gene expression underlying the performance of an extreme vocal behavior, the courtship hum of the plainfin midshipman fish (Porichthys notatus). Single hums can last up to two hours and may be repeated throughout an evening of courtship activity. We asked whether vocal behavioral states are associated with specific gene expression signatures in key brain regions that regulate vocalization by comparing transcript levels in humming versus non-humming males. We find that the circadian-related genes period3 and Clock are significantly upregulated in the vocal motor nucleus and preoptic area-anterior hypothalamus, respectively, in humming compared to non-humming males, indicating that internal circadian clocks may differ between these divergent behavioral states. In addition, we identify suites of differentially expressed genes related to synaptic transmission, ion channels and transport, hormone signaling, and metabolism and antioxidant activity that may permit or support humming behavior. These results underscore the importance of the known circadian control of midshipman humming and provide testable candidate genes for future studies of the neuroendocrine and motor control of energetically demanding courtship behaviors in midshipman fish and other vertebrate groups.

Regulation of sleep homeostasis by sexual arousal

In all animals, sleep pressure is under continuous tight regulation. It is universally accepted that this regulation arises from a two-process model, integrating both a circadian and a homeostatic controller. Here we explore the role of environmental social signals as a third, parallel controller of sleep homeostasis and sleep pressure. We show that, in Drosophila melanogaster males, sleep pressure after sleep deprivation can be counteracted by raising their sexual arousal, either by engaging the flies with prolonged courtship activity or merely by exposing them to female pheromones.

Detection of predator cues alters mating tactics in male wolf spiders

Males of the wolf spider, Rabidosa punctulata, exhibit condition-dependent alternative mating tactics, whereby small, poor condition males engage in multimodal courtship while large, good condition males adopt a direct mount tactic that forgoes courtship. This study explores the possibility that tactic-specific costs can help explain this unintuitive pattern of mating tactic expression. Specifically, we hypothesize that courtship signaling is costly with respect to eavesdropping by predators and that males can alter their tactic expression based upon the perceived environmental predation risk. We test this by first examining the risk of predation associated with different mating tactics. We use a co-occurring predatory heterospecific, R. rabida as our predator. We found support for the prediction that courting R. punctulata males tended to be attacked more often than non-courting males, and the likelihood of being attacked was best predicted by courtship activity. Given this documented cost, we hypothesized that R. punctulata males would adjust their mating tactic based upon perceived predation risk. In a second experiment, we manipulated perceived predation risk by providing R. punctulata males with different female silk cues (conspecific; predatory heterospecific; conspecific + predatory heterospecific) and examined mating tactic expression. In support of our hypothesis, males were more likely to adopt the direct mount tactic in the presence of predatory heterospecific or mixed silk cues and were more likely to court in the presence of conspecific cues. These results support the hypothesis that the cost of predation from eavesdroppers may influence the evolution and expression of male alternative mating tactics in R. punctulata.

Spinal Motor and Sensory Neurons Are Androgen Targets in an Acrobatic Bird

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 (3H-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.

Social behavior and sexual dimorphism in the Bonaire whiptail, Cnemidophorus murinus (Squamata: Teiidae): the role of sexual selection

We measured body dimensions and coloration and quantified the behavior of females and males of two color phases in the Bonaire whiptail, Cnemidophorus murinus, to begin addressing the ultimate causation for sexual dimorphism in this species. Examination of size-adjusted body dimensions revealed that males have wider, longer, and deeper heads as well as somewhat longer forelegs and hind legs. Males were characterized by two distinct coloration patterns. Blue males displayed purple–blue dewlaps, blue–gray background coloration on the head and anterior torso, numerous light blue spots on the flanks, brown–orange coloration on the posterior torso, and a turquoise section on the proximal portion of the tail. By contrast, brown males were uniform olive–green to yellow–brown, with the exception of light blue spots on the lateral torso. Females were colored like brown males but lacked the blue spots. Testis length scaled with body size. Testes of only 26% of brown males were active, whereas all blue males had active testes. Blue males initiated aggressive encounters involving chases and displays directed toward other males much more frequently than females were aggressive with consexuals or with either type of male. Brown males were not observed to initiate aggression. Most blue male aggression was directed toward other blue males (70.6% of encounters), whereas 29.4% of encounters were with brown males. Blue males initiated 85.7% of the courtship encounters observed compared with only 7.1% initiated by brown males and 7.2% by females. Male-biased dimorphism in head and leg dimensions as well as coloration, together with higher rates of intrasexual aggression and courtship activity by blue males, are consistent with the hypothesis that sexual selection explains the evolution of sexual dimorphism in C. murinus.