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The melanocortin system is a neuroendocrine machinery that has been associated with phenotypic diversification in a number of vertebrate lineages. Central to the highly pleiotropic melanocortin system is the pro-opiomelanocortin (pomc) gene family, a family of pre-prohormones that each give rise to melanocyte stimulating hormone (MSH), adrenocorticotropic releasing hormone (ACTH), ??-lipotropin hormone, and ??-endorphin. Here we examine the structure, tissue expression profile, and pattern of cis transcriptional regulation of the three pomc paralogs (??1, ??2, and ??) in the model cichlid fish Astatotilapia burtoni and other cichlids, teleosts, and mammals. We found that the hormone-encoding regions of pomc ??1, pomc ??2 and pomc ?? are highly conserved, with a few notable exceptions. Surprisingly, the pomc ?? gene of cichlids and pomacentrids (damselfish) encodes a novel melanocortin peptide, ??-MSH, as a result of a tandem duplication of the segment encoding ACTH. All three genes are expressed in the brain and peripheral tissues, but pomc ??1 and ??2 show a more spatially restricted expression profile than pomc ??. In addition, the promoters of each pomc gene have diverged in nucleotide sequence, which may have facilitated the diverse tissue-specific expression profiles of these paralogs across species. Increased understanding of the mechanisms regulating pomc gene expression will be invaluable to the study of pomc in the context of phenotypic evolution. ?? 2013 Elsevier Inc.

Across animals, there is remarkable diversity in behavior. Modern genomic approaches have made it possible to identify the molecular underpinnings of varied behavioral phenotypes. By examining species with plastic phenotypes we have begun to understand the dynamic and flexible nature of neural transcriptomes and identified gene modules associated with variation in social and reproductive behaviors in diverse species. Importantly, it is becoming increasingly clear that some candidate genes and gene networks are involved in complex social behaviors across even divergent species, yet few comparative transcriptomics studies have been conducted that examine a specific behavior across species. We discuss the implications of a range of important and insightful studies that have increased our understanding of the neurogenomics of behavioral plasticity. Despite its successes, behavioral genomics has been criticized for its lack of hypotheses and causative insights. We propose here a novel avenue to overcome some of these short-comings by complementing “forward genomics” studies (i.e., from phenotype to behaviorally relevant gene modules) with a “reverse genomics” approach (i.e., manipulating novel gene modules to examine effects on behavior, hormones, and the genome itself) to examine the functional causes and consequences of differential gene expression patterns. We discuss how several established approaches (such as pharmacological manipulations of a novel candidate pathway, fine scale mapping of novel candidate gene expression in the brain, or identifying direct targets of a novel transcription factor of interest) can be used in combination with the analysis of the accompanying neurogenomic responses to reveal unexpected biological processes. The integration of forward and reverse genomics will move the field beyond statistical associations and yield great insights into the neural and molecular control of social behavior and its evolution.

An individual’s position in a social hierarchy profoundly affects behavior and physiology through interactions with community members, yet little is known about how the brain contributes to status differences between and within the social states or sexes. We aimed to determine sex-specific attributes of social status by comparing circulating sex steroid hormones and neural gene expression of sex steroid receptors in dominant and subordinate male and female Astatotilapia burtoni, a highly social African cichlid fish. We found that testosterone and 17??-estradiol levels are higher in males regardless of status and dominant individuals regardless of sex. Progesterone was found to be higher in dominant individuals regardless of sex. Based on pharmacological manipulations in males and females, progesterone appears to be a common mechanism for promoting courtship in dominant individuals. We also examined expression of androgen receptors, estrogen receptor ??, and the progesterone receptor in five brain regions that are important for social behavior. Most of the differences in brain sex steroid receptor expression were due to sex rather than status. Our results suggest that the parvocellular preoptic area is a core region for mediating sex differences through androgen and estrogen receptor expression, whereas the progesterone receptor may mediate sex and status behaviors in the putative homologs of the nucleus accumbens and ventromedial hypothalamus. Overall our results suggest sex differences and similarities in the regulation of social dominance by gonadal hormones and their receptors in the brain. ?? 2013 Elsevier Inc.

Steroid hormones play an important role in modulating behavioral responses to various social stimuli. It has been suggested that variation in the hormonal regulation of behavior across species is associated with social organization and/or mating system. In order to further elucidate the interplay of hormones and behavior in social situations, we exposed males of the monogamous convict cichlid Amatitliana nigrofasciata to three social stimuli: gravid female, intruder male, and a nonsocial stimulus. We used a repeated measure design to create behavioral profiles and explore how sex steroid hormones respond to and regulate social behavior. Results show distinct behavioral responses to different social situations, with circulating 11-ketotestosterone increasing in response to social stimuli. Pharmacological manipulations using specific androgen and estrogen receptor agonists and antagonists exposed complex control over digging behavior in the social opportunity context. In the social challenge context, aggressive behaviors decreased in response to blocking the androgen receptor pathway. Our results extend our understanding of sex steroid regulation of behavioral responses to social stimulation. ?? 2013 Elsevier Inc.

Understanding how complex organisms function as integrated units that constantly interact with their environment is a long-standing chal- lenge in biology. To address this challenge, organismal biology reveals general organizing principles of physiological systems and behavior—in particular, in complex multicellular animals. Organismal biology also focuses on the role of individual variability in the evolutionary main- tenance of diversity. To broadly advance these frontiers, cross-compatibility of experimental designs, methodological approaches, and data interpretation pipelines represents a key prerequisite. It is now possible to rapidly and systematically analyze complete genomes to elucidate genetic variation associated with traits and conditions that define individuals, populations, and species. However, genetic variation alone does not explain the varied individual physiology and behavior of complex organisms. We propose that such emergent properties of complex organisms can best be explained through a renewed emphasis on the context and life-history dependence of individual phenotypes to comple- ment genetic data.

Hormones play an important role in the regulation of reproductive behavior. Here, we examined the effects of the fatty acid derivative prostaglandin F2α (PGF2) on female sexual behavior as well as the interaction between PGF2-induced mating behavior with male courtship display in the lek-breeding African cichlid fish, Astatotilapia burtoni. In a two-way choice paradigm, we found that nonreproductive females preferred to associate with smaller, less aggressive males over larger, more aggressive males. However, PGF2-treated females dramatically reversed their preference to larger males. In a second experiment, PGF2 treatment dramatically increased sexual behavior in nonreproductive females as measured by time spent in the bower of the stimulus male, even when the female and the stimulus male were separated by a transparent divider. This effect was even more pronounced when the stimulus males were exposed to the putative female pheromone 17α,20β-progesterone (17α,20β-P). Under full-contact conditions, only PGF2-treated females visited a stimulus male’s bower, where they even displayed circling behavior usually only seen during spawning. Interestingly, male performance prior to PGF2 treatment predicted female sexual response. Our study demonstrates the importance of PGF2 in the control of female reproductive behavior in interaction with male performance.

Neuroendocrine pathways that regulate social behavior are remarkably conserved across divergent taxa. The neuropeptides arginine vasotocin/vasopressin (AVT/AVP) and their receptor V1a mediate aggression, space use, and mating behavior in male vertebrates. The hormone prolactin (PRL) also regulates social behavior across species, most notably paternal behavior. Both hormone systems may be involved in the evolution of monogamous mating systems. We compared AVT, AVT receptor V1a2, PRL, and PRL receptor PRLR1 gene expression in the brains as well as circulating androgen concentrations of free-living reproductively active males of two closely related North American cichlid species, the monogamous Herichthys cyanoguttatus and the polygynous Herichthys minckleyi. We found that H. cyanoguttatus males bond with a single female and together they cooperatively defend a small territory in which they reproduce. In H. minckleyi, a small number of large males defend large territories in which they mate with several females. Levels of V1a2 mRNA were higher in the hypothalamus of H. minckleyi, and PRLR1 expression was higher in the hypothalamus and telencephalon of H. minckleyi. 11-ketotestosterone levels were higher in H. minckleyi, while testosterone levels were higher in H. cyanoguttatus. Our results indicate that a highly active AVT/V1a2 circuit(s) in the brain is associated with space use and social dominance and that pair bonding is mediated either by a different, less active AVT/V1a2 circuit or by another neuroendocrine system. ?? 2013 Elsevier Inc.

Individuals integrate information about their environment into adaptive behavioural responses, yet how different sensory modalities contribute to these decisions and where in the brain this integration occurs is not well understood. We presented male cichlid fish (Astatotilapia burtoni) with sensory information in three social contexts: intruder challenge, reproductive opportunity and a socially neutral situation. We then measured behavioural and hormonal responses along with induction of the immediate early gene c-Fos in candidate forebrain regions. In the intruder challenge context, males were exposed to either a visual stimulus of a dominant male, the putative male pheromone androstenedione, or both. We found that, compared to the neutral context, a visual stimulus was necessary and sufficient for an aggressive response, whereas both chemical and visual stimuli were needed for an androgen response. In the reproductive opportunity context, males were exposed to either a visual stimulus of a receptive female, a progesterone metabolite (female pheromone) only, or both. We further found that the visual stimulus is necessary and sufficient for an androgen response in the reproductive opportunity context. In the brain, we observed c-Fos induction in response to a visual challenge stimulus specifically in dopaminergic neurones of area Vc (the central region of the ventral telencephalon), a putative striatal homologue, whereas presentation of a chemical stimulus did not induce c-Fos induction in the intruder challenge context. Our results suggest that different sensory cues are processed in a social context-specific manner as part of adaptive decision-making processes.

The roles of estrogen and androgens in male social behavior are well studied, but little is known about how these hormones contribute to behavior in a social hierarchy. Here we test the role of aromatase, the enzyme that converts testosterone into estradiol, in mediating aggression and reproductive behavior in male Astatotilapia burtoni, an African cichlid fish that displays remarkable plasticity in social behavior. We first measured aromatase expression in subordinate and dominant males in brain regions that regulate social behavior and found that subordinate males have higher aromatase expression than dominant males in the magnocellular and gigantocellular regions of the preoptic area. Next, we functionally tested the role of aromatase in regulating behavior by intraperitoneally injecting dominant males with either saline or fadrozole (FAD), an aromatase inhibitor, and found that FAD treatment decreases aggressive, but not reproductive, behaviors compared to saline controls. To determine the underlying physiological and molecular consequences of FAD treatment, we measured estradiol and testosterone levels from plasma and brain aromatase expression in FAD and saline treated dominant males. We found that estradiol levels decreased and testosterone levels increased in response to FAD treatment. Moreover, FAD treated males had increased aromatase expression in the gigantocellular portion of the POA, possibly a compensatory response. Overall, our results suggest aromatase is a key enzyme that promotes aggression in A. burtoni males through actions in the preoptic area. ?? 2013 Elsevier Inc.