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Social environment can affect the expression of sex-typical behavior in both males and females. Males of the African cichlid species Astatotilapia burtoni have long served as a model system to study the neural, endocrine, and molecular basis of socially plastic dominance behavior. Here we show that in all-female communities of A. burtoni, some individuals acquire a male-typical dominance phenotype, including aggressive territorial defense, distinctive color patterns, and courtship behavior. Furthermore, dominant females have higher levels of circulating androgens than either subordinate females or females in mixed-sex communities. These male-typical traits do not involve sex change, nor do the social phenotypes in all-female communities differ in relative ovarian size, suggesting that factors other than gonadal physiology underlie much of the observed variation. In contrast to the well-studied situation in males, dominant and subordinate females do not differ in the rate of somatic growth. Dominant females are not any more likely than subordinates to spawn with an introduced male, although they do so sooner. These results extend the well known extraordinary behavioral plasticity of A. burtoni to the females of this species and provide a foundation for uncovering the neural and molecular basis of social dominance behavior while controlling for factors such as sex, gonadal state and growth. ?? 2012 Elsevier Inc.

Social status strongly affects behavior and physiology, in part mediated by gonadal hormones, although how each sex steroid acts across levels of biological organization is not well understood. We examine the role of sex steroids in modulating social behavior in dominant (DOM) and subordinate (SUB) males of a highly social fish, Astatotilapia burtoni. We first used agonists and antagonists to each sex steroid receptor and found that androgens and progestins modulate courtship behavior only in DOM, whereas estrogens modulate aggressive behavior independent of social status. We then examined the hormonal and physiological responses to sex steroid receptor antagonist treatment and uncovered substantial changes in circulating steroid hormone levels and gonad size only in SUB, not in DOM. Consistent with status-based physiological sensitivities to drug manipulation, we found that neuropeptide and steroid receptor gene expression in the preoptic area was sensitive only in SUB. However, when we compared the transcriptomes of males that received either vehicle or an estrogen receptor antagonist, 8.25% of all genes examined changed expression in DOM in comparison with only 0.56% in SUB. Finally, we integrate behavior, physiology, and brain gene expression to infer functional modules that underlie steroid receptor regulation of behavior. Our work suggests that environmentally induced changes at one level of biological organization do not simply affect changes of similar magnitude at other levels, but that instead very few key pathways likely serve as conduits for executing plastic responses across multiple levels.

Sexual selection on male coloration has been implicated in the evolution of colourful species flocks of East African cichlid fish. During adaptive radiations, animals diverge in multiple phenotypic traits, but the role of physiology has received limited attention. Here, we report how divergence in physiology may contribute to the stable coexistence of two hybridizing incipient species of cichlid fish from Lake Victoria. Males of Pundamilia nyererei (males are red) tend to defeat those of Pundamilia pundamilia (males are blue), yet the two sibling species coexist in nature. It has been suggested that red males bear a physiological cost that might offset their dominance advantage. We tested the hypothesis that the two species differ in oxidative stress levels and immune function and that this difference is correlated with differences in circulating steroid levels. We manipulated the social context and found red males experienced significantly higher oxidative stress levels than blue males, but only in a territorial context when colour and aggression are maximally expressed. Red males exhibited greater aggression levels and lower humoral immune response than blue males, but no detectable difference in steroid levels. Red males appear to trade off increased aggressiveness with physiological costs, contributing to the coexistence of the two species. Correlated divergence in colour, behaviour and physiology might be widespread in the dramatically diverse cichlid radiations in East African lakes and may play a crucial role in the remarkably rapid speciation of these fish.

Previous winning experience increases the probability of winning a subsequent contest. However, it is not clear whether winning probability is affected only by the outcome of the contest (winning or losing) or whether fighting experience itself is also sufficient to induce this effect. We investigated this question in the East African cichlid fish Pundamilia spec. To create an unresolved conflict we allowed males to fight their own mirror image prior to a real fight against a size-matched non-mirror-stimulated control male. When males fight their own mirror image, the image’s response corresponds to the action of the focal animal, creating symmetrical fighting conditions without the experience of losing or winning. We found that mirror-stimulated males were more likely to win an ensuing contest than control males. Interestingly, in this species mirror stimulation also induced an increase in circulating androgens, which is consistent with the hypothesis that stimulation of these sex steroids during aggressive encounters may prepare the animal for subsequent encounters. Our results suggest that fighting experience alone coupled with an androgen response, increases the likelihood of winning, even in the absence of a winning experience. ?? 2011 Elsevier Inc.

All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation. J. Comp. Neurol. 519:3599–3639, 2011. © 2011 Wiley-Liss, Inc.

The present study describes the distribution of an arginine vasotocin (AVT) V1a receptor (AVTr) throughout the brain of a sex-changing grouper, rock hind Epinephelus adscensionis. The objectives of this study were to describe the AVTr distribution in the brain of rock hind for potential linkages of the AVT hormone system with sex-specific behaviors observed in this species and to examine sex-specific differences that might exist. An antibody was designed for rock hind AVTr against the deduced amino acid sequence for the third intracellular loop. Protein expression, identified with immunohistochemistry showed high concordance with mRNA expression, identified with in situ hybridization. AVTr protein and mRNA expression was widely distributed throughout the brain, indicating that AVT may act as a neuromodulator via this V1a receptor subtype. AVTr protein and mRNA were present in regions associated with behavior, reproduction and spatial learning, as well as sensory functions such as vision, olfaction and lateral line sensory processing. We observed high AVTr expression in granular cell formations in the internal cellular layer of olfactory bulbs, torus longitudinalis, granular layer of the corpus cerebellum, valvula of the cerebellum, nuclei of the lateral and posterior recesses, and granular eminence. High protein and mRNA expression was also observed in the preoptic area, anterior hypothalamus, and habenular nucleus. No obvious sex differences were noted in any region of the rock hind brain. ?? 2011 Elsevier B.V.

Social life affects brain function at all levels, including gene expression, neurochemical balance, and neural circuits. We have previously shown that in the cichlid fish Astatotilapia burtoni brightly colored, socially dominant (DOM) males face a trade-off between reproductive opportunities and increased predation risk. Compared with camouflaged subordinate (SUB) males, DOMs exposed to a loud sound pip display higher startle responsiveness and increased excitability of the Mauthner cell (M-cell) circuit that governs this behavior. Using behavioral tests, intracellular recordings, and single-cell molecular analysis, we show here that serotonin (5-HT) modulates this socially regulated plasticity via the 5-HT receptor subtype 2 (5-HTR(2)). Specifically, SUBs display increased sensitivity to pharmacological manipulation of 5-HTR(2) compared with DOMs in both startle-escape behavior and electrophysiological properties of the M-cell. Immunohistochemistry showed serotonergic varicosities around the M-cells, further suggesting that 5-HT impinges directly onto the startle-escape circuitry. To determine whether the effects of 5-HTR(2) are pre- or postsynaptic, and whether other 5-HTR subtypes are involved, we harvested the mRNA from single M-cells via cytoplasmic aspiration and found that 5-HTR subtypes 5A and 6 are expressed in the M-cell. 5-HTR(2), however, was absent, suggesting that it affects M-cell excitability through a presynaptic mechanism. These results are consistent with a role for 5-HT in modulating startle plasticity and increase our understanding of the neural and molecular basis of a trade-off between reproduction and predation.

The nonapeptides arginine vasopressin (AVP; including its non-mammalian homolog arginine vasotocin, AVT) and oxytocin (OT; including its non-mammalian homologs mesotocin, MT, and isotocin, IT) regulate social behavior, including aggression and reproduction, via receptors conserved across vertebrates. In monogamous prairie voles, the vasopressin and oxytocin pathways are crucially important for pair-bond formation, specifically by influencing affiliative behavior toward the mate and aggression toward non-mates. Monogamous social systems are found in diverse taxa. We hypothesized that the AVT/IT pathways are associated with mating behavior in monogamous teleost fishes. We used the monogamous convict cichlid, Amatitlania nigrofasciata, to test this idea. In the first experiment, we treated males with a general nonapeptide receptor antagonist during pair-bond formation. Control males were treated with vehicle. On the first day of treatment we observed a significant reduction in both affiliative behavior toward the potential mate and aggression toward neighbors. However, the antagonist did not prevent the pair-bond from forming and the behavioral effects disappeared on subsequent treatment days. In the second experiment, we administered on three consecutive days the AVP/OT receptor antagonist to males that were in an established pair-bond. In established pairs, male affiliation towards the mate and aggressive behavior towards territorial neighbors were not affected by the antagonist. Our results indicate that the basic social behaviors typically mediated by the AVP/OT pathways may provide the building blocks necessary for monogamous mating behavior. ?? 2010 Elsevier Inc.

The gonadal steroid hormone progesterone plays an important role across all vertebrates in mediating female reproductive physiology and behavior. Many effects of progesterone are mediated by a nuclear progesterone receptor (PR), which is crucial for integration of external signals and internal physiological cues in the brain to produce an appropriate behavioral output. The t??ngara frog, Physalaemus pustulosus, is an excellent model system for the study of mechanisms by which sensory signals, such as auditory communication, are processed within neural circuits where mate choice decisions are made. To establish a framework for studying the neural basis of mate choice and social behavior in this species, we first describe the cytoarchitecture of the brain using Nissl-stained sections. Then, in order to better understand where progesterone acts to regulate social decisions, we determined the distribution of PR protein throughout the brain of P. pustulosus by immunohistochemistry. We found PR immunoreactivity in key brain regions known to modulate the processing of auditory cues and social behavior in other vertebrates. Due to its widespread distribution, PR likely also plays important roles in non-limbic brain regions that mediate non-social information processing. Further, we have colocalized PR with tyrosine hydroxylase, providing a functional context for the role of progesterone in mediating motivation and motor behavior. Our results significantly extend our understanding of hormonal modulation in the anuran brain and support the important role of the nuclear progesterone receptor in modulating female mate choice and receptivity in amphibians and across vertebrates. ?? 2011 Elsevier B.V.

Tremendous progress has been made in our understanding of the ultimate and proximate mechanisms underlying social behavior, yet an integrative evolutionary analysis of its underpinnings has been difficult. In this review, we propose that modern genomic approaches can facilitate such studies by integrating four approaches to brain and behavior studies: (1) animals face many challenges and opportunities that are ecologically and socially equivalent across species; (2) they respond with species-specific, yet quantifiable and comparable approach and avoidance behaviors; (3) these behaviors in turn are regulated by gene modules and neurochemical codes; and (4) these behaviors are governed by brain circuits such as the mesolimbic reward system and the social behavior network. For each approach, we discuss genomic and other studies that have shed light on various aspects of social behavior and its underpinnings and suggest promising avenues for future research into the evolution of neuroethological systems. ?? 2010 Elsevier Inc.