Mechanosensory signaling as a potential mode of communication during social interactions in fishes

© 2016. Published by The Company of Biologists Ltd. Signals produced during social interactions convey crucial information about the sender\u27s identity, quality, reproductive state and social status. Fishes can detect near-body water movements via the mechanosensory lateral line system, and this sense is used during several common fish behaviors, such as schooling, rheotaxis and predator-prey interactions. In addition, many fish behaviors, such as aggressive lateral displays and reproductive body quivers, involve fin and body motions that generate water movements that can be detected by the lateral line system of nearby fish. This mechanosensory system is well studied for its role in obstacle avoidance and detection of inadvertent hydrodynamic cues generated during schooling and predator-prey interactions; however, little research has focused on the role of mechanosensory communication during social interactions. Here, we summarize the current literature on the use of mechanosensation-mediated behaviors during agonistic and reproductive encounters, as well as during parental care. Based on these studies, we hypothesize that mechanosensory signaling is an important but often overlooked mode of communication during conspecific social interactions in many fish species, and we highlight its importance during multimodal communication. Finally, we suggest potential avenues of future research that would allow us to better understand the role of mechanosensation in fish communication

Underwater noise impairs social communication during aggressive and reproductive encounters

© 2020 The Association for the Study of Animal Behaviour Human-generated noise pollution is of global concern, as designated by the World Health Organization (WHO, 2011, Burden of disease from environmental noise: Quantification of healthy life years lost in Europe. https://www.who.int/quantifying_ehimpacts/publications/e94888/en/). Increases in shipping, sonar use, pile driving, and more have all contributed to a rise in ambient underwater sound levels. Unfortunately, continuous low-intensity sounds, like shipping noise, are pervasive in shallow-shore environments where many social species live and correspond to the frequency ranges at which many fishes produce and detect acoustic stimuli. Noise has the potential to alter the sender\u27s production of the signal, mask the signal itself (if acoustic), or change the receiver\u27s physiology. We hypothesized that continuous tonal noise would impair social interactions and communication. To test this, we used highly social African cichlid fish, Astatotilapia burtoni, to examine inter- and intrasexual interactions that occurred in a control or noisy environment (pure tones of 100–2000 Hz). During reproductive interactions, we found that males changed the location of their courtship behaviours. Instead of producing courtship quivers (and associated sounds) immediately next to gravid females, males produced these behaviours inside their spawning shelter. This change in location decreases the likelihood of the female detecting it. Also detrimental to acoustic communication, we found that noise-exposed gravid females had lower hearing sensitivity at 100–200 Hz, a major component of male courtship sounds. In addition, males changed their visual displays during male–male territorial interactions such that they spent more time with their eyebar displayed, suggesting an increase in visual signalling. Together, these data indicate that noise may impact all three components of social communication: signal production, signal reception and the signal itself, and highlights a possible cross-modal impact of noise on visual signalling. Subtle changes to social behaviours and communication, rather than dramatic effects such as injury or mortality, are important to evaluating sublethal impacts of noise on reproductive success and species survival

The mechanosensory lateral line system mediates activation of socially-relevant brain regions during territorial interactions

© 2016 Butler and Maruska. Animals use multiple senses during social interactions and must integrate this information in the brain to make context-dependent behavioral decisions. For fishes, the largest group ofvertebrates, the mechanosensory lateral line system provides crucial hydrodynamic information for survival behaviors, but little is known about its function in social communication. Our previous work using the African cichlid fish, Astatotilapia burtoni, provided the first empirical evidence that fish use their lateral line system to detect water movements from conspecifics for mutual assessment and behavioral choices. It is unknown, however, where this socially-relevant mechanosensory information is processed in the brain to elicit adaptive behavioral responses. To examine for the first time in any fish species which brain regions receive contextual mechanosensory information, we quantified expression ofthe immediate early gene cfos as a proxy for neural activation in sensory and socially-relevant brain nuclei from lateral line-intact and -ablated fish following territorial interactions. Our in situ hybridization results indicate that in addition to known lateral line processing regions, socially-relevant mechanosensory information is processed in the ATn (ventromedial hypothalamus homolog), Dl (putative hippocampus homolog), and Vs (putative medial extended amygdala homolog). In addition, we identified a functional network within the conserved social decision-making network (SDMN) whose co-activity corresponds with mutual assessment and behavioral choice. Lateral line-intact and -ablated fight winners had different patterns of co-activity of these function networks and group identity could be determined solely by activation patterns, indicating the importance of mechanoreception to co-activity of the SDMN. These data show for the first time that the mechanosensory lateral line system provides relevant information to conserved decision-making centers of the brain during territorial interactions to mediate crucial behavioral choices such as whether or not to engage in a territorial fight. To our knowledge, this is also the first evidence of a subpallial nucleus receiving mechanosensory input, providing important information for elucidating homologies of decision-making circuits across vertebrates. These novel results highlight the importance ofconsidering multimodal sensory input in mediating context-appropriate behaviors that will provide broad insights on the evolution of decision-making networks across all taxa

The mechanosensory lateral line is used to assess opponents and mediate aggressive behaviors during territorial interactions in an African cichlid fish

© 2015. Published by The Company of Biologists Ltd. Fish must integrate information from multiple sensory systems to mediate adaptive behaviors. Visual, acoustic and chemosensory cues provide contextual information during social interactions, but the role of mechanosensory signals detected by the lateral line system during aggressive behaviors is unknown. The aim of this study was first to characterize the lateral line system of the African cichlid fish Astatotilapia burtoni and second to determine the role of mechanoreception during agonistic interactions. The A. burtoni lateral line system is similar to that of many other cichlid fishes, containing lines of superficial neuromasts on the head, trunk and caudal fin, and narrow canals. Astatotilapia burtoni males defend their territories from other males using aggressive behaviors that we classified as non-contact or contact. By chemically and physically ablating the lateral line system prior to forced territorial interactions, we showed that the lateral line system is necessary for mutual assessment of opponents and the use of non-contact fight behaviors. Our data suggest that the lateral line system facilitates the use of noncontact assessment and fight behaviors as a protective mechanism against physical damage. In addition to a role in prey detection, the diversity of lateral line morphology in cichlids may have also enabled the expansion of their social behavioral repertoire. To our knowledge, this is the first study to implicate the lateral line system as a mode of social communication necessary for assessment during agonistic interactions

Localization of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish, Astatotilapia burtoni

© 2016 Wiley Periodicals, Inc. Neural communication depends on release and reception of different neurotransmitters within complex circuits that ultimately mediate basic biological functions. We mapped the distribution of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish Astatotilapia burtoni using in situ hybridization to label vesicular glutamate transporters (vglut1, vglut2.1, vglut3), glutamate decarboxylases (gad1, gad2), and choline acetyltransferase (chat). Cells expressing the glutamatergic markers vgluts 1–3 show primarily nonoverlapping distribution patterns, with the most widespread expression observed for vglut2.1, and more restricted expression of vglut1 and vglut3. vglut1 is prominent in granular layers of the cerebellum, habenula, preglomerular nuclei, and several other diencephalic, mesencephalic, and rhombencephalic regions. vglut2.1 is widely expressed in many nuclei from the olfactory bulbs to the hindbrain, while vglut3 is restricted to the hypothalamus and hindbrain. GABAergic cells show largely overlapping gad1 and gad2 expression in most brain regions. GABAergic expression dominates nuclei of the subpallial ventral telencephalon, while glutamatergic expression dominates nuclei of the pallial dorsal telencephalon. chat-expressing cells are prominent in motor cranial nerve nuclei, and some scattered cells lie in the preoptic area and ventral part of the ventral telencephalon. A localization summary of these markers within regions of the conserved social decision-making network reveals a predominance of either GABAergic or glutamatergic cells within individual nuclei. The neurotransmitter distributions described here in the brain of a single fish species provide an important resource for identification of brain nuclei in other fishes, as well as future comparative studies on circuit organization and function. J. Comp. Neurol. 525:610–638, 2017. © 2016 Wiley Periodicals, Inc

Reproductive and metabolic state differences in olfactory responses to amino acids in a mouth brooding African cichlid fish

© 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology. Olfaction mediates many crucial life-history behaviors such as prey detection, predator avoidance, migration and reproduction. Olfactory function can also be modulated by an animal\u27s internal physiological and metabolic states. While this is relatively well studied in mammals, little is known about how internal state impacts olfaction in fishes, the largest and most diverse group of vertebrates. Here we apply electroolfactograms (EOGs) in the African cichlid fish Astatotilapia burtoni to test the hypothesis that olfactory responses to food-related cues (i.e. L-amino acids; alanine and arginine) vary with metabolic, social and reproductive state. Dominant males (reproductively active, reduced feeding) had greater EOG magnitudes in response to amino acids at the same tested concentration than subordinate males (reproductively suppressed, greater feeding and growth rates). Mouth brooding females, which are in a period of starvation while they brood fry in theirmouths, had greater EOGmagnitudes in response to amino acids at the same tested concentration than both recovering and gravid females that are feeding. Discriminant function analysis on EOG magnitudes also grouped the male (subordinate) and female (recovering, gravid) phenotypes with higher food intake together and distinguished them from brooding females and dominant males. The slope of the initial negative phase of the EOG also showed intra-sexual differences in both sexes.Our results demonstrate that the relationship between olfaction and metabolic state observed in other taxa is conserved to fishes. For the first time, we provide evidence for intrasexual plasticity in the olfactory response to amino acids that is influenced by fish reproductive, social and metabolic state

Distribution of aromatase in the brain of the African cichlid fish Astatotilapia burtoni: Aromatase expression, but not estrogen receptors, varies with female reproductive-state

© 2020 Wiley Periodicals, Inc. 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

Neural and behavioural correlates of repeated social defeat

© 2018 The Author(s). Dominance hierarchies are common across the animal kingdom and have important consequences for reproduction and survival. Animals of lower social status cope with repeated social defeat using proactive and reactive behaviours. However, there remains a paucity of information on how an individual\u27s coping behaviours changes over time or what neural mechanisms are involved. We used a resident-intruder paradigm in the African cichlid fish Astatotilapia burtoni to investigate the neural correlates of these two opposing behaviour groups. Fish initially used both proactive and reactive behaviours, but had a dramatic increase in use of proactive behaviours during the third interaction, and this was followed by cessation of proactive behaviours and exclusive use of reactive coping. By quantifying neural activation in socially-relevant brain regions, we identify a subset of brain nuclei, including those homologous to the mammalian amygdala, showing higher activation in fish displaying proactive but not reactive behaviours. Fish displaying reactive behaviours had greater neural activation in the superior raphe, suggesting a possible conserved function during social defeat across vertebrates. These data provide the first evidence on the involvement of specific brain regions underlying proactive and reactive coping in fishes, indicating that these nuclei have conserved functions during social defeat across taxa