Search for: All records

Parental care is important for offspring survival and success. Recognition of offspring by parents is critical to ensure parents direct care behaviors at related offspring and minimize energy lost by caring for unrelated young. Offspring recognition of parents prevents possible aggressive interactions between young and unrelated adults and allows offspring to direct begging behaviors toward the correct adult. Despite its importance and widespread nature, much of the current research has focused on a small range of species, particularly mammals and birds. We review the existing literature on the sensory mechanisms of parent-offspring recognition in fishes, amphibians, and reptiles. Within these groups, there is diversity in the presence and strategies for parent-offspring recognition. Future studies should continue to identify these mechanisms, as well as the neural and endocrine underpinnings in non-model organisms to expand our knowledge of this behavior and inform our understanding of the evolution of parent-offspring recognition.

 

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. 

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. 

Nitric oxide (NO) produced by the enzyme neuronal nitric oxide synthase serves as an important neurotransmitter in the central nervous system that is involved in reproductive regulation, learning, sensory processing, and other forms of neural plasticity. Here, we map the distribution ofnnos‐expressing cells in the brain and retina of the cichlid fishAstatotilapia burtoniusing in situ hybridization. In the brain,nnos‐expressing cells are found from the olfactory bulbs to the hindbrain, including within specific nuclei involved in decision‐making, sensory processing, neuroendocrine regulation, and the expression of social behaviors. In the retina,nnos‐expressing cells are found in the inner nuclear layer, presumably in amacrine cells. We also used quantitative PCR to test for differences innnosexpression within the eye and olfactory bulbs of males and females of different reproductive states and social statuses. In the eye, males express morennosthan females, and socially dominant males express morennosthan subordinate males, but expression did not differ among female reproductive states. In the olfactory bulbs, dominant males had greaternnosexpression than subordinate males. These results suggest a status‐specific function for NO signaling in the visual and olfactory systems that may be important for sensory perception related to mating or territorial interactions to maintain the social hierarchy. The widespread distribution ofnnos‐expressing cells throughout the cichlid brain is similar to that in other teleosts, with some conserved localization patterns across vertebrates, suggesting diverse functions for this important neurotransmitter system.

 

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.

 

The ability to identify odors in the environment is crucial for survival and reproduction. However, whether olfactory processing in higher-order brain centers is influenced by an animal’s physiological condition is unknown. We usedin vivoneuron and local field potential (LFP) recordings from the ventral telencephalon of dominant and subordinate male cichlids to test the hypothesis that response properties of olfactory neurons differ with social status. Dominant males had a high percentage of neurons that responded to several odor types, suggesting broad tuning or differential sensitivity when males are reproductively active and defending a territory. A greater percentage of neurons in dominant males also responded to sex- and food-related odors, while a greater percentage of neurons in subordinate males responded to complex odors collected from behaving dominant males, possibly as a mechanism to mediate social suppression and allow subordinates to identify opportunities to rise in rank. Odor-evoked LFP spectral densities, indicative of synaptic inputs, were also 2–3-fold greater in dominant males, demonstrating status-dependent differences in processing possibly linking olfactory and other neural inputs to goal-directed behaviors. For the first time we reveal social and reproductive-state plasticity in olfactory processing neurons in the vertebrate forebrain that are associated with status-specific lifestyles.

 

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.

 

Neurokinin B, encoded by thetachykinin3gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamictac3expression for its role in reproduction, but detailed studies on extra‐hypothalamictac3expression are limited. Here, we identified twotac3genes in the social African cichlid fishAstatotilapia burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization fortac3amRNA identified cell populations throughout the brain. Numeroustac3acells 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,tac3expression was absent from the pituitary. Using double‐fluorescent staining, we localizedtac3a‐expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH‐tac3acolabeled cells were observed, dense GnRH fibers surround and potentially synapse withtac3acells in the preoptic area. Only minimal (<5%) colabeling oftac3awas observed inkiss2cells. Despitetac3aexpression in many nodes of the mesolimbic reward system, it was absent from tyrosine hydroxylase (TH)‐expressing cells, buttac3acells 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.