Social Transitions Cause Rapid Behavioral and Neuroendocrine Changes

© 2015 The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. In species that form dominance hierarchies, there are often opportunities for low-ranking individuals to challenge high-ranking ones, resulting in a rise or fall in social rank. How does an animal rapidly detect, process, and then respond to these social transitions? This article explores and summarizes how these social transitions can rapidly (within 24 h) impact an individual\u27s behavior, physiology, and brain, using the African cichlid fish, Astatotilapia burtoni, as a model. Male A. burtoni form hierarchies in which a few brightly-colored dominant males defend territories and spawn with females, while the remaining males are subordinate, more drab-colored, do not hold a territory, and have minimal opportunities for reproduction. These social phenotypes are plastic and reversible, meaning that individual males may switch between dominant and subordinate status multiple times within a lifetime. When the social environment is manipulated to create males that either ascend (subordinate to dominant) or descend (dominant to subordinate) in rank, there are rapid changes in behavior, circulating hormones, and levels of gene expression in the brain that reflect the direction of transition. For example, within minutes, males ascending in status show bright coloration, a distinct eye-bar, increased dominance behaviors, activation of brain nuclei in the social behavior network, and higher levels of sex steroids in the plasma. Ascending males also show rapid changes in levels of neuropeptide and steroid receptors in the brain, as well as in the pituitary and testes. To further examine hormone-behavior relationships in this species during rapid social ascent, the present study also measured levels of testosterone, 11-ketotestosterone, estradiol, progestins, and cortisol in the plasma during the first week of social ascent and tested for correlations with behavior. Plasma levels of all steroids were rapidly increased at 30 min after social ascent, but were not correlated with behavior during the initial rise in rank, suggesting that behavior is dissociated from endocrine status. These changes during social ascent are then compared with our current knowledge about males descending in rank, who rapidly show faded coloration, decreased dominance behaviors, increased subordinate behaviors, and higher circulating levels of cortisol. Collectively, this work highlights how the perception of similar social cues that are opposite in value are rapidly translated into adaptive behavioral and neuroendocrine changes that promote survival and reproductive fitness. Finally, future directions are proposed to better understand the mechanisms that govern these rapid changes in social position

Social regulation of reproduction in male cichlid fishes

© 2014 Elsevier Inc. Social interactions and relative positions within a dominance hierarchy have helped shape the evolution of reproduction in many animals. Since reproduction is crucial in all animals, and rank typically regulates access to reproductive opportunities, understanding the mechanisms that regulate socially-induced reproductive processes is extremely important. How does position in a dominance hierarchy impact an individual\u27s reproductive behavior, morphology, and physiology? Teleost fishes, and cichlids in particular, are ideally-suited models for studying how social status influences reproduction on multiple levels of biological organization. Here I review the current knowledge on the reproductive behavioral and physiological consequences of relative position in a dominance hierarchy, with a particular focus on male cichlids. Dominant and subordinate social status is typically associated with distinct differences in activity along the entire hypothalamic-pituitary-gonadal axis. Further, when transitions in social status occur between subordinate and dominant individuals, there are plastic changes from whole-organism behavior to molecular-level gene expression modifications that occur quickly. These rapid changes in behavior and physiology have allowed cichlids the flexibility to adapt to and thrive in their often dynamic physical and social environments. Studies in cichlid fishes have, and will continue, to advance our understanding of how the social environment can modulate molecular, cellular, and behavioral outcomes relevant to reproductive success. Future studies that take advantage of the extreme diversity in mating systems, reproductive tactics, and parental care strategies within the cichlid group will help generate hypotheses and careful experimental tests on the mechanisms governing the social control of reproduction in many vertebrates

Context-dependent chemosensory signaling, aggression and neural activation patterns in gravid female African cichlid fish

© 2017. Published by The Company of Biologists Ltd . Social animals must constantly assess their environment to make appropriate behavioral decisions. The use of various sensory modalities is imperative in this process and it is hypothesized that the highly conserved brain nuclei comprising the social decisionmaking network (SDMN) integrates social information with an animal\u27s internal state to elicit behavioral responses. Here, we used the highly social African cichlid fish, Astatotilapia burtoni, to investigate whether reproductively receptive (gravid) females show contextual chemosensory signaling, social behaviors and neural activation patterns within the SDMN. We exposed gravid females to different social contexts: (1) dominant male (inter-sexual reproductive); (2) mouth brooding (non-receptive) female; (3) gravid female (intra-sexual aggressive); (4) juvenile fish (low social salience); and (5) empty compartment (control). By injecting females with a blue dye to visualize urine pulses, we found that gravid females show context-dependent urination, exhibiting higher urination rates in the presence of dominant males (reproductive context) and mouth brooding females (aggressive contexts). Further, gravid females show contextual aggression with increased aggressive displays toward mouth brooding females compared with other gravid females. Using in situ hybridization to quantify cells expressing the immediate early gene cfos as a measure of neural activation, we also show that certain regions of the SDMN in gravid females are differentially activated after exposure to high compared with low social salience contexts. Coupled with previous reports, these results demonstrate true chemosensory communication in both sexes of a single fish species, as well as reveal the neural substrates mediating intra-and inter-sexual social behaviors in females

Three Distinct Glutamate Decarboxylase Genes in Vertebrates

Gamma-aminobutyric acid (GABA) is a widely conserved signaling molecule that in animals has been adapted as a neurotransmitter. GABA is synthesized from the amino acid glutamate by the action of glutamate decarboxylases (GADs). Two vertebrate genes, GAD1 and GAD2, encode distinct GAD proteins: GAD67 and GAD65, respectively. We have identified a third vertebrate GAD gene, GAD3. This gene is conserved in fishes as well as tetrapods. We analyzed protein sequence, gene structure, synteny, and phylogenetics to identify GAD3 as a homolog of GAD1 and GAD2. Interestingly, we found that GAD3 was lost in the hominid lineage. Because of the importance of GABA as a neurotransmitter, GAD3 may play important roles in vertebrate nervous systems

A second corticotropin-releasing hormone gene (CRH2) is conserved across vertebrate classes and expressed in the hindbrain of a basal Neopterygian fish, the spotted gar (Lepisosteus oculatus)

© 2015 Wiley Periodicals, Inc. To investigate the origins of the vertebrate stress-response system, we searched sequenced vertebrate genomes for genes resembling corticotropin-releasing hormone (CRH). We found that vertebrate genomes possess, in addition to CRH, another gene that resembles CRH in sequence and syntenic environment. This paralogous gene was previously identified only in the elephant shark (a holocephalan), but we find it also in marsupials, monotremes, lizards, turtles, birds, and fishes. We examined the relationship of this second vertebrate CRH gene, which we name CRH2, to CRH1 (previously known as CRH) and urocortin1/urotensin1 (UCN1/UTS1) in primitive fishes, teleosts, and tetrapods. The paralogs CRH1 and CRH2 likely evolved via duplication of CRH during a whole-genome duplication early in the vertebrate lineage. CRH2 was subsequently lost in both teleost fishes and eutherian mammals but retained in other lineages. To determine where CRH2 is expressed relative to CRH1 and UTS1, we used in situ hybridization on brain tissue from spotted gar (Lepisosteus oculatus), a neopterygian fish closely related to teleosts. In situ hybridization revealed widespread distribution of both crh1 and uts1 in the brain. Expression of crh2 was restricted to the putative secondary gustatory/secondary visceral nucleus, which also expressed calcitonin-related polypeptide alpha (calca), a marker of parabrachial nucleus in mammals. Thus, the evolutionary history of CRH2 includes restricted expression in the brain, sequence changes, and gene loss, likely reflecting release of selective constraints following whole-genome duplication. The discovery of CRH2 opens many new possibilities for understanding the diverse functions of the CRH family of peptides across vertebrates

Divergent evolution of two corticotropin-releasing hormone (CRH) genes in teleost fishes

© 2015 Grone and Maruska. Genome duplication, thought to have happened twice early in vertebrate evolution and a third time in teleost fishes, gives rise to gene paralogs that can evolve subfunctions or neofunctions via sequence and regulatory changes. To explore the evolution and functions of corticotropin-releasing hormone (CRH), we searched sequenced teleost genomes for CRH paralogs. Our phylogenetic and synteny analyses indicate that two CRH genes, crha and crhb, evolved via duplication of crh1 early in the teleost lineage. We examined the expression of crha and crhb in two teleost species from different orders: an African cichlid, Burton\u27s mouthbrooder, (Astatotilapia burtoni; Order Perciformes) and zebrafish (Danio rerio; Order Cypriniformes). Furthermore, we compared expression of the teleost crha and crhb genes with the crh1 gene of an outgroup to the teleost clade: the spotted gar (Lepisosteus oculatus). In situ hybridization for crha and crhb mRNA in brains and eyes revealed distinct expression patterns for crha in different teleost species. In the cichlid, crha mRNA was found in the retina but not in the brain. In zebrafish, however, crha mRNA was not found in the retina, but was detected in the brain, restricted to the ventral hypothalamus. Spotted gar crh1 was found in the retina as well as the brain, suggesting that the ancestor of teleost fishes likely had a crh1 gene expressed in both retina and brain. Thus, genome duplication may have freed crha from constraints, allowing it to evolve distinct sequences, expression patterns, and likely unique functions in different lineages

Directional sound sensitivity in utricular afferents in the toadfish Opsanus tau

© 2015 Published by The Company of Biologists Ltd. The inner ear of fishes contains three paired otolithic end organs, the saccule, lagena and utricle, which function as biological accelerometers. The saccule is the largest otolith in most fishes and much of our current understanding on auditory function in this diverse group of vertebrates is derived from anatomical and neurophysiological studies on this end organ. In contrast, less is known about how the utricle contributes to auditory functions. In this study, chronically implanted electrodes were used, along with neural telemetry or tethers to record primary afferent responses from the utricular nerve in free-ranging and naturally behaving oyster toadfish Opsanus tau Linnaeus. The hypothesis was that the utricle plays a role in detecting underwater sounds, including conspecific vocalizations, and exhibits directional sensitivity. Utricular afferents responded best to low frequency (80-200 Hz) pure tones and to playbacks of conspecific boatwhistles and grunts (80-180 Hz fundamental frequency), with the majority of the units (∼75%) displaying a clear, directional response, which may allow the utricle to contribute to sound detection and localization during social interactions. Responses were well within the sound intensity levels of toadfish vocalization (approximately 140 SPL dBrms re. 1 μPa with fibers sensitive to thresholds of approximately 120 SPL dBrms re. 1 μPa). Neurons were also stimulated by self-generated body movements such as opercular movements and swimming. This study is the first to investigate underwater sound-evoked response properties of primary afferents from the utricle of an unrestrained/ unanesthetized free-swimming teleost fish. These data provide experimental evidence that the utricle has an auditory function, and can contribute to directional hearing to facilitate sound localization

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

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

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