Sex differences and similarities in the neuroendocrine regulation of social behavior in an African cichlid fish ☆ , ☆☆ Lauren A. O'Connell a,b,1 , Julia H. Ding b , Hans A. Hofmann a,b,c, ⁎ a Institute for Cell and Molecular Biology, University of Texas at Austin, Austin, TX 78705, USA b Section of Integrative Biology, University of Texas at Austin, Austin, TX 78705, USA c Institute for Neuroscience, University of Texas at Austin, Austin, TX 78705, USA abstract article info Article history: Received 22 June 2013 Accepted 21 July 2013 Available online 28 July 2013 Keywords: Social behavior Estrogen Estrogen receptor Androgen Androgen receptor Progesterone Progesterone receptor Aggression Reproduction 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 subordi- nate male and female Astatotilapia burtoni, a highly social African cichlid fish. We found that testosterone and 17β-estradiol levels are higher in males regardless of status and dominant individuals regardless of sex. Proges- terone was found to be higher in dominant individuals regardless of sex. Based on pharmacological manipula- tions 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 α, and the proges- terone 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. All rights reserved. Introduction In many social species, members of a community form dominance hierarchies where social status profoundly affects an individual's behavior and physiology through interactions with community mem- bers (Sapolsky, 2005). The physiological basis of social dominance is often associated with differences in reproductive status and sex steroid hormone levels (Wingfield et al., 1991), which make studying the molecular determinants of social dominance difficult to dissect from reproductive physiology. Moreover, little is known about how these physiological and behavioral differences are integrated within the brain. In order to disentangle sex-specific physiology from the neuroen- docrine mechanisms of social dominance, we utilized a highly social fish that has plastic behavioral phenotypes and readily forms dominance hierarchies within community tanks. Males of the cichlid fish Astatotilapia burtoni display phenotypic plasticity in social status, alternating between dominant (DOM) and subordinate (SUB) phenotypes depending on the social environment. DOM males are conspicuously colored, reproduc- tively active, and aggressively defend territories where they court and spawn with females. SUB males are dull in coloration, school with females, and are reproductively inactive. Although neuroendocrine differences between DOM and SUB males have been described in vari- ous contexts (Maruska and Fernald, 2010a; O'Connell and Hofmann, 2012), disentangling the neural basis of social dominance from differ- ences in reproductive status is difficult. Female A. burtoni provide an excellent opportunity to dissect the mechanisms of social status from reproductive state, as females will also form dominance hierarchies in the absence of males, but both DOM and SUB females are reproductively active (Renn et al., 2012). By comparing DOM and SUB males and fe- males, we have a unique opportunity to determine to which extent the neuroendocrine underpinnings of behavior within a social hierarchy are due to either reproductive state or social status. In order to function in a social community that is based on a domi- nance hierarchy, individuals must integrate external social information Hormones and Behavior 64 (2013) 468–476 ☆ Grant Sponsor: NSF DDIG 1011253 to LAO, University Co-op Undergraduate Fellowship to JHD, and NSF grant IOS 0843712, the Alfred P. Sloan Foundation, and a Dwight W. and Blanche Faye Reeder Centennial Fellowship in Systematic and Evolutionary Biology to HAH. ☆☆ Disclosure statement: The authors have nothing to disclose. ⁎ Corresponding author at: Section of Integrative Biology, The University of Texas at Austin, 1 University Station, C0930, Austin, TX 78712, USA. Fax: +1 512 471 3878. E-mail address: hans@mail.utexas.edu (H.A. Hofmann). 1 Current address: FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USA. 0018-506X/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yhbeh.2013.07.003 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh