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  1. Synopsis

    Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared with non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g., sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared with mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.

     
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  2. Abstract Animal communication signals are regulated by multiple hormonal axes that ensure appropriate signal targeting, timing, and information content. The regulatory roles of steroid hormones and many peptide hormones are well understood and documented across a wide range of vertebrate taxa. Two recent studies have reported a novel function for leptin, a peptide hormone central to energy balance regulation: regulating communication signals of weakly electric fish and singing mice. With only limited evidence available at this time, a key question is just how widespread leptinergic regulation of communication signals is within and across taxa. A second important question is what features of communication signals are subject to leptinergic regulation. Here, we consider the functional significance of leptinergic regulation of animal communication signals in the context of both direct and indirect signal metabolic costs. Direct costs arise from metabolic investment in signal production, while indirect costs arise from the predation and social conflict consequences of the signal's information content. We propose a preliminary conceptual framework for predicting which species will exhibit leptinergic regulation of their communication signals and which signal features leptin will regulate. This framework suggests a number of directly testable predictions within and across taxa. Accounting for additional factors such as life history and the potential co-regulation of communication signals by leptin and glucocorticoids will likely require modification or elaboration of this model. 
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  3. Synopsis Most animals experience reproductive transitions in their lives; for example, reaching reproductive maturity or cycling in and out of breeding condition. Some reproductive transitions are abrupt, while others are more gradual. In most cases, changes in communication between the sexes follow the time course of these reproductive transitions and are typically thought to be coordinated by steroid hormones. We know a great deal about hormonal control of communication behaviors in birds and frogs, as well as the central neural control of these behaviors. There has also been significant interest in the effects of steroid hormones on central nervous system structures that control both the production and reception of communication signals associated with reproductive behaviors. However, peripheral sensory structures have typically received less attention, although there has been growing interest in recent years. It is becoming clear that peripheral sensory systems play an important role in reproductive communication, are plastic across reproductive conditions, and, in some cases, this plasticity may be mediated by steroid hormones. In this article, we discuss recent evidence for the role of peripheral auditory structures in reproductive communication in birds and frogs, the plasticity of the peripheral auditory system, and the role of steroid hormones in mediating the effects of the peripheral auditory system on reproductive communication. We focus on both seasonal and acute reproductive transitions, introduce new data on the role of hormones in modulating seasonal patterns, and make recommendations for future work. 
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  4. Abstract Animal communication requires senders to transmit signals through the environment to conspecific receivers, which then leads to context-dependent behavioral decisions. Sending and receiving sensory information in social contexts, however, can be dramatically influenced by an individual’s internal state, particularly in species that cycle in and out of breeding or other physiological condition like nutritional state or social status. Modulatory substances like steroids, peptides, and biogenic amines can influence both the substrates used for sending social signals (e.g., motivation centers, sensorimotor pathways, and muscles) as well as the peripheral sensory organs and central neural circuitry involved in the reception of this information and subsequent execution of behavioral responses. This issue highlights research from neuroethologists on the topic of modulation of sending and receiving social signals and demonstrates that it can occur in both males and females, in different senses at both peripheral sensory organs and the brain, at different levels of biological organization, on different temporal scales, in various social contexts, and across many diverse vertebrate taxa. Modifying a signal produced by a sender or how that signal is perceived in a receiver provides flexibility in communication and has broad implications for influencing social decisions like mate choice, which ultimately affects reproductive fitness and species persistence. This phenomenon of modulators and internal physiological state impacting communication abilities is likely more widespread than currently realized and we hope this issue inspires others working on diverse systems to examine this topic from different perspectives. An integrative and comparative approach will advance discovery in this field and is needed to better understand how endocrine modulation contributes to sexual selection and the evolution of animal communication in general. 
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  5. Abstract In seasonally breeding vertebrates, hormones coordinate changes in nervous system structure and function to facilitate reproductive readiness and success. Steroid hormones often exert their effects indirectly via regulation of neuromodulators, which in turn can coordinate the modulation of sensory input with appropriate motor output. Female plainfin midshipman fish (Porichthys notatus) undergo increased peripheral auditory sensitivity in time for the summer breeding season, improving their ability to detect mates, which is regulated by steroid hormones. Reproductive females also show differences in catecholaminergic innervation of auditory circuitry compared with winter, non-reproductive females as measured by tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholaminergic synthesis. Importantly, catecholaminergic input to the inner ear from a dopaminergic-specific forebrain nucleus is decreased in the summer and dopamine inhibits the sensitivity of the inner ear, suggesting that gonadal steroids may alter auditory sensitivity by regulating dopamine innervation. In this study, we gonadectomized non-reproductive females, implanted them with estradiol (E2) or testosterone (T), and measured TH immunoreactive (TH-ir) fibers in auditory nuclei where catecholaminergic innervation was previously shown to be seasonally plastic. We found that treatment with T, but not E2, reduced TH-ir innervation in the auditory hindbrain. T-treatment also reduced TH-ir fibers in the forebrain dopaminergic cell group that projects to the inner ear, and likely to the auditory hindbrain. Higher T plasma in the treatment group was correlated with reduced-ir TH terminals in the inner ear. These T-treatment induced changes in TH-ir fibers mimic the seasonal downregulation of dopamine in the midshipman inner ear and provide evidence that steroid hormone regulation of peripheral auditory sensitivity is mediated, in part, by dopamine. 
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  6. Synopsis Intra- and inter-sexual communications are vital to the survival and reproductive success of animals. In species that cycle in and out of breeding or other physiological condition, sensory function can be modulated to optimize communication at crucial times. Little is known, however, about how widespread this sensory plasticity is across taxa, whether it occurs in multiple senses or both sexes within a species, and what potential modulatory substances and substrates are involved. Thus, studying modulation of sensory communication in a single species can provide valuable insights for understanding how sensory abilities can be altered to optimize detection of salient signals in different sensory channels and social contexts. The African cichlid fish Astatotilapia burtoni uses multimodal communication in social contexts such as courtship, territoriality, and parental care and shows plasticity in sensory abilities. In this review, we synthesize what is known about how visual, acoustic, and chemosensory communication is used in A. burtoni in inter- and intra-specific social contexts, how sensory funtion is modulated by an individual’s reproductive, metabolic, and social state, and discuss evidence for plasticity in potential modulators that may contribute to changes in sensory abilities and behaviors. Sensory plasticity in females is primarily associated with the natural reproductive cycle and functions to improve detection of courtship signals (visual, auditory, chemosensory, and likely mechanosensory) from high-quality males for reproduction. Plasticity in male sensory abilities seems to function in altering their ability to detect the status of other males in the service of territory ownership and future reproductive opportunities. Changes in different classes of potential modulators or their receptors (steroids, neuropeptides, and biogenic amines) occur at both peripheral sensory organs (eye, inner ear, and olfactory epithelium) and central visual, olfactory, and auditory processing regions, suggesting complex mechanisms contributing to plasticity of sensory function. This type of sensory plasticity revealed in males and females of A. burtoni is likely more widespread among diverse animals than currently realized, and future studies should take an integrative and comparative approach to better understand the proximate and ultimate mechanisms modulating communication abilities across taxa. 
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  7. Synopsis Although hormonally-derived female sex pheromones have been well described in approximately a dozen species of teleost fish, only a few male sex pheromones have been characterized and the neuroendocrine underpinnings of behavioral responsiveness to them is not understood. Herein, we describe a study that addresses this question using the goldfish, Carassius auratus, an important model species of how hormones drive behavior in egg-laying teleost fishes. Our study had four components. First, we examined behavioral responsiveness of female goldfish and found that when injected with prostaglandin F2α (PGF2α), a treatment that drives female sexual receptivity, and found that they became strongly and uniquely attracted to the odor of conspecific mature males, while non-PGF2α-treated goldfish did not discern males from females. Next, we characterized the complexity and specificity of the male pheromone by examining the responsiveness of PGF2α-treated females to the odor of either mature male conspecifics or male common carp odor, as well as their nonpolar and polar fractions. We found that the odor of male goldfish was more attractive than that of male common carp, and that its activity was attributable to both its nonpolar and polar fractions with the later conveying information on species-identity. Third, we hypothesized that androstenedione (AD), a 19-carbon sex steroid produced by all male fish might be the nonpolar fraction and tested whether PGF2α-treated goldfish were attracted to either AD alone or as part of a mixture in conspecific water. We found that while AD was inactive on its own, it became highly attractive when added to previously unattractive female conspecific water. Lastly, in a test of whether nonhormonal conspecific odor might determine species-specificity, we added AD to water of three species of fish and found that while AD made goldfish water strongly attractive, its effects on other species holding water were small. We conclude that circulating PGF2α produced at the time of ovulation induces behavioral sensitivity to a male sex pheromone in female goldfish and that this male pheromone is comprised of AD and a mixture of body metabolites. Because PGF2α commonly mediates ovulation and female sexual behavior in egg-laying fishes, and AD is universally produced by male fishes as a precursor to testosterone, we suggest that these two hormones may have similar roles mediating male–female behavior and communication in many species of fish. 
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  8. Synopsis Adrenal glucocorticoids (GCs) are increasingly recognized as important modulators of male courtship signals, suggesting that circulating levels of these steroids can play a central role in sexual selection. However, few studies have examined whether GC-mediated effects on male sexual signals actually impact mate choice by females. Here, we examine how corticosterone (CORT)-mediated changes in the vocalizations of male green treefrogs, Dryophytes cinereus, influence attractiveness to females. In this species, agonistic acoustic signaling between rival males competing for mates increases circulating CORT levels in contest losers. Acute elevations in CORT, in turn, decrease the duration of male advertisement calls and increase the latency between successive calls, resulting in a net reduction in vocal effort (the amount of signaling per unit time) that occurs independently of changes in circulating androgens. Based on known preferences for acoustic features in D. cinereus, and other anuran species, the direction of CORT-mediated effects on temporal call characteristics is expected to compromise attractiveness to females, but whether they are of sufficient magnitude to impact female mate choice decisions is unclear. To examine whether CORT-mediated effects on male advertisement calls reduce attractiveness to females, we broadcast vocalizations in dual speaker playback experiments approximating the mean and 1 SD above and below the mean call duration and vocal effort values (the two primary vocal features impacted by elevated CORT) of males with low and high CORT levels. Results revealed strong preferences by females for the calls characteristic of males with low CORT in tests using the approximate mean and 1 SD above the mean call duration and vocal effort values, but females did not show a preference for calls of males with low CORT in trials using call values approximating 1 SD below the mean. Overall, females preferred males with signal traits predictive of low CORT, however this effect was nonlinear with attenuated preferences when signal alternatives differed only marginally indicating a possible thresholding effect. Specifically, females appeared to discriminate between males with low versus high CORT based primarily on differences in call rates associated with CORT-mediated changes in call duration and vocal effort. Our results highlight that changes in circulating CORT during male–male vocal interactions can decrease attractiveness to females, suggesting that circulating levels of CORT can play a critical role in both intra- and intersexual selection. 
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  9. Synopsis Lizards use chemical communication to mediate many reproductive, competitive, and social behaviors, but the neuroendocrine mechanisms underlying chemical communication in lizards are not well understood and understudied. By implementing a neuroendocrine approach to the study of chemical communication in reptiles, we can address a major gap in our knowledge of the evolutionary mechanisms shaping chemical communication in vertebrates. The neuropeptide arginine vasotocin (AVT) and its mammalian homolog vasopressin are responsible for a broad spectrum of diversity in competitive and reproductive strategies in many vertebrates, mediating social behavior through the chemosensory modality. In this review, we posit that, though limited, the available data on AVT-mediated chemical communication in lizards reveal intriguing patterns that suggest AVT plays a more prominent role in lizard chemosensory behavior than previously appreciated. We argue that these results warrant more research into the mechanisms used by AVT to modify the performance of chemosensory behavior and responses to conspecific chemical signals. We first provide a broad overview of the known social functions of chemical signals in lizards, the glandular sources of chemical signal production in lizards (e.g., epidermal secretory glands), and the chemosensory detection methods and mechanisms used by lizards. Then, we review the locations of vasotocinergic populations and neuronal projections in lizard brains, as well as sites of peripheral receptors for AVT in lizards. Finally, we end with a case study in green anoles (Anolis carolinensis), discussing findings from recently published work on the impact of AVT in adult males on chemosensory communication during social interactions, adding new data from a similar study in which we tested the impact of AVT on chemosensory behavior of adult females. We offer concluding remarks on addressing several fundamental questions regarding the role of AVT in chemosensory communication and social behavior in lizards. 
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  10. Abstract Although mate searching behavior in female túngara frogs (Physalaemus pustulosus) is nocturnal and largely mediated by acoustic cues, male signaling includes visual cues produced by the vocal sac. To compensate for these low light conditions, visual sensitivity in females is modulated when they are in a reproductive state, as retinal thresholds are decreased. This study tested whether estradiol (E2) plays a role in this modulation. Female túngara frogs were injected with either human chorionic gonadotropin (hCG) or a combination of hCG and fadrozole. hCG induces a reproductive state and increases retinal sensitivity, while fadrozole is an aromatase inhibitor that blocks hCG-induced E2 synthesis. In an analysis of scotopic electroretinograms (ERGs), hCG treatment lowered the threshold for eliciting a b-wave response, whereas the addition of fadrozole abolished this effect, matching thresholds in non-reproductive saline-injected controls. This suggests that blocking E2 synthesis blocked the hCG-mediated reproductive modulation of retinal sensitivity. By implicating E2 in control of retinal sensitivity, our data add to growing evidence that the targets of gonadal steroid feedback loops include sensory receptor organs, where stimulus sensitivity may be modulated, rather than more central brain nuclei, where modulation may affect mechanisms involved in motivation. 
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