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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.more » « less
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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.more » « less
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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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Abstract Nonapeptides play a crucial role in mediating reproduction, aggression, and parental care across taxa. In fishes,
arginine vasotocin (AVT) expression is related to social and/or reproductive status in most male fishes studied to date, and is linked to territorial defense, paternal care, and courtship. Despite a plethora of studies examining AVT in male fishes, relatively little is known about how AVT expression varies with female reproductive state or its role in female social behaviors. We used multiple methods for examining the AVT system in female African cichlid fishAstatotilapia burtoni , including immunohistochemistry for AVT, in situ hybridization foravt ‐mRNA, and quantitative PCR. Ovulated and mouthbrooding females had similar numbers of parvocellular, magnocellular, and gigantocellular AVT cells in the preoptic area. However, ovulated females had larger magnocellular and gigantocellular cells compared to mouthbrooding females, and gigantocellular AVT cell size correlated with the number of days brooding, such that late‐stage brooding females had larger AVT cells than mid‐stage brooding females. In addition, we found that ventral hypothalamic cells were more prominent in females compared to males, and were larger in mouthbrooding compared to ovulated females, suggesting a role in maternal care. Together, these data indicate that AVT neurons change across the reproductive cycle in female fishes, similar to that seen in males. These data on females complement studies in maleA .burtoni , providing a comprehensive picture of the regulation and potential function of different AVT cell types in reproduction and social behaviors in both sexes. -
ABSTRACT Neurokinin B, encoded by the
tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamictac3 expression for its role in reproduction, but detailed studies on extra‐hypothalamictac3 expression are limited. Here, we identified twotac3 genes in the social African cichlid fishAstatotilapia burtoni , only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization fortac3a mRNA identified cell populations throughout the brain. Numeroustac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scatteredtac3 ‐expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts,tac3 expression was absent from the pituitary. Using double‐fluorescent staining, we localizedtac3a ‐expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH‐tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse withtac3a cells in the preoptic area. Only minimal (<5%) colabeling oftac3a was observed inkiss2 cells. Despitetac3a expression in many nodes of the mesolimbic reward system, it was absent from tyrosine hydroxylase (TH)‐expressing cells, buttac3a cells were located in areas with dense TH fibers. The presence oftac3a ‐expressing cells throughout the brain, including in socially relevant brain regions, suggest more diverse functions beyond regulation of reproductive physiology that may be conserved across vertebrates. -
Abstract Estrogen synthesis and signaling in the brains of vertebrates has pleotropic effects ranging from neurogenesis to modulation of behaviors. The majority of studies on brain‐derived estrogens focus on males, but estrogenic signaling in females likely plays important roles in regulation of reproductive cycling and social behaviors. We used females of the mouth brooding African cichlid fish,
Astatotilapia burtoni , to test for reproductive state‐dependent changes in estrogenic signaling capacity within microdissected brain nuclei that are important for social behaviors. Expression levels of the rate‐limiting enzyme aromatase, but not estrogen receptors, measured by qPCR changes across the reproductive cycle. Gravid females that are close to spawning had higher aromatase levels in all brain regions compared to females with lower reproductive potential. This brain aromatase expression was positively correlated with circulating estradiol levels and ovarian readiness. Using chromogenic in situ hybridization we localized aromatase‐expressing cells to ependymal regions bordering the ventricles from the forebrain to the hindbrain, and observed more abundant staining in gravid compared to mouth brooding females in most regions. Staining was most prominent in subpallial telencephalic regions, and diencephalic regions of the preoptic area, thalamus, and hypothalamus, but was also observed in sensory and sensorimotor areas of the midbrain and hindbrain. Aromatase expression was observed in radial glial cells, revealed by co‐localization with the glial marker GFAP and absence of co‐localization with the neuronal marker HuC/D. Collectively these results support the idea that brain‐derived estradiol in females may serve important functions in reproductive state‐dependent physiological and behavioral processes across vertebrates.