Social regulation of male reproductive plasticity in an African cichlid fish

Social interactions with the outcome of a position in a dominance hierarchy can have profound effects on reproductive behavior and physiology, requiring animals to integrate environmental information with their internal physiological state; but how is salient information from the animal\u27s dynamic social environment transformed into adaptive behavioral, physiological, and molecular-level changes? The African cichlid fish, Astatotilapia burtoni, is ideally suited to understand socially controlled reproductive plasticity because activity of the male reproductive (brainpituitary gonad) axis is tightly linked to social status. Males form hierarchies in which a small percentage of brightly colored dominant individuals have an active reproductive axis, defend territories, and spawn with females, while the remaining males are subordinate, drably colored, do not hold a territory, and have a suppressed reproductive system with minimal opportunities for spawning. These social phenotypes are plastic and quickly reversible, meaning that individual males may switch between dominant and subordinate status multiple times within a lifetime. Here, we review the rapid and remarkable plasticity that occurs along the entire reproductive axis when males rise in social rank, a transition that has important implications for the operational sex ratio of the population. When males rise in rank, transformations occur in the brain, pituitary, circulation, and testes over short time-scales (minutes to days). Changes are evident in overt behavior, as well as modifications at the physiological, cellular, and molecular levels that regulate reproductive capacity. Widespread changes triggered by a switch in rank highlight the significance of external social information in shaping internal physiology and reproductive competence. © The Author 2013. All rights reserved

Behavioral and physiological plasticity: Rapid changes during social ascent in an African cichlid fish

In many vertebrates, reproduction is regulated by social interactions in which dominant males control access to females and food. Subordinate males that displace dominant individuals must rapidly adopt behavioral and physiological traits of the higher rank to gain reproductive success. To understand the process of phenotypic plasticity during social ascent, we analyzed the temporal expression pattern of dominance behaviors and circulating androgen levels when socially-suppressed males of an African cichlid fish Astatotilapia burtoni ascended in status. These experiments tested a prediction of the \u27challenge hypothesis\u27 that, during periods of social instability, male androgen levels are higher than during socially stable times. We found that socially and reproductively suppressed males perform territorial and reproductive behaviors within minutes of an opportunity to ascend in status, and that animals switch from initial expression of territorial behaviors to more reproductive behaviors during territory establishment. Following this rapid response, social stability may be achieved within 1-3. days of social ascent. Consistent with predictions of the \u27challenge hypothesis\u27, circulating 11-ketotestosterone (11-KT) levels were elevated within 30. min following social opportunity, coincident with increased aggressive behavior. However, territorial behaviors and serum 11-KT levels were then dissociated by 72. h after social ascent, suggesting either rapid social stability and/or increased physiological potential for androgen production. This behavioral and physiological plasticity in male A. burtoni suggests that perception of social opportunity triggers a suite of quick changes to facilitate rapid transition towards reproductive success, and reveals important features of social ascent not previously recognized. © 2010 Elsevier Inc

Reproductive status regulates expression of sex steroid and GnRH receptors in the olfactory bulb

Neuromodulators including gonadotropin-releasing hormone (GnRH) and sex steroids help integrate an animal\u27s internal physiological state with incoming external cues, and can have profound effects on the processing of behaviorally relevant information, particularly from the olfactory system. While GnRH and steroid receptors are present in olfactory processing regions across vertebrates, little is known about whether their expression levels change with internal physiological state or external social cues. We used qRT-PCR to measure mRNA levels of two GnRH receptors (GnRH-R1, GnRH-R2), five sex steroid receptors (estrogen receptors: ERα, ERβa, ERβb; androgen receptors: ARα, ARβ), and aromatase in the olfactory bulb of the highly social African cichlid fish Astatotilapia burtoni. We asked whether these receptor levels changed with reproductive condition in females, or with social status, which regulates reproductive capacity in males. Our results reveal that mRNA levels of multiple sex steroid, GnRH receptor subtypes, and aromatase in the olfactory bulb vary with sex, social status in males, and reproductive condition in females, which highlights the potential importance of changing receptor levels in fine-tuning the olfactory system during the reproductive cycle. Further, steroid receptor mRNA levels were positively correlated with circulating steroid levels in males, but negatively correlated in females, suggesting different regulatory control between sexes. These results provide support for the hypothesis that the first-order olfactory relay station is a substrate for both GnRH and sex steroid modulation, and suggest that changes in receptor levels could be an important mechanism for regulating reproductive, social, and seasonal plasticity in olfactory perception observed across vertebrates. © 2010 Elsevier B.V

Contextual chemosensory urine signaling in an African cichlid fish

Chemosensory signaling is crucial for communication in many fish species, but little is known about how signalers modulate chemical output in response to sensory information and social context. Here, we tested the hypothesis that dominant male African cichlid fish (Astatotilapia burtoni) use urine signals during social interactions, and demonstrate that this signaling depends on social context (reproductive; territorial) and on available sensory information (visual cues; full interaction). We injected males with dye to visualize urine pulses and exposed them to full sensory information or visual cues alone of four types: (1) dominant male; (2) gravid (reproductively receptive) females; (3) mouth-brooding (non-receptive) females; or (4) control (no fish). We found that males released urine sooner and increased their urination frequency when visually exposed to gravid females as compared with mouth-brooding females and or no-fish controls. While males could distinguish female reproductive states using visual cues alone, courtship behavior rates were ̃10-fold higher when they fully interacted with gravid females compared with receiving visual cues alone. Males also increased their urination and territorial behaviors when exposed to another male, suggesting that chemical signals may convey information on dominance status. These data support the hypothesis that dominant males use urine as a chemical signal and adjust the frequency of their urine output based on contextual information. © 2012. Published by The Company of Biologists Ltd

Mechanistic target of rapamycin (mTOR) implicated in plasticity of the reproductive axis during social status transitions

© 2019 Elsevier Inc. The highly conserved brain-pituitary-gonadal (BPG) axis controls reproduction in all vertebrates, so analyzing the regulation of this signaling cascade is important for understanding reproductive competence. The protein kinase mechanistic target of rapamycin (mTOR) functions as a conserved regulator of cellular growth and metabolism in all eukaryotes, and also regulates the reproductive axis in mammals. However, whether mTOR might also regulate the BPG axis in non-mammalian vertebrates remains unexplored. We used complementary experimental approaches in an African cichlid fish, Astatotilapia burtoni, to demonstrate that mTOR is involved in regulation of the brain, pituitary, and testes when males rise in rank to social dominance. mTOR or downstream components of its signaling pathway (p-p70S6K) were detected in gonadotropin-releasing hormone (GnRH1) neurons, the pituitary, and testes. Transcript levels of mtor in the pituitary and testes also varied when reproductively-suppressed subordinate males rose in social rank to become dominant reproductively-active males, a transition similar to puberty in mammals. Intracerebroventricular injection of the mTORC1 inhibitor, rapamycin, revealed a role for mTOR in the socially-induced hypertrophy of GnRH1 neurons. Rapamycin treatment also had effects at the pituitary and testes, suggesting involvement of the mTORC1 complex at multiple levels of the reproductive axis. Thus, we show that mTOR regulation of BPG function is conserved to fishes, likely playing important roles in regulating reproduction and fertility across all male vertebrates

Characterization of cell proliferation throughout the brain of the African cichlid fish Astatotilapia burtoni and its regulation by social status

New cells are added in the brains of all adult vertebrates, but fishes have some of the greatest potential for neurogenesis and gliogenesis among all taxa, partly due to their indeterminate growth. Little is known, however, about how social interactions influence cell proliferation in the brain of these fishes that comprise the largest group of vertebrates. We used 5-bromo-2′-deoxyuridine (BrdU) to identify and localize proliferation zones in the telencephalon, diencephalon, mesencephalon, and rhombencephalon that were primarily associated with ventricular surfaces in the brain of the African cichlid fish Astatotilapia burtoni. Cell migration was evident in some regions by 1 day post injection, and many newborn cells coexpressed the neuronal marker HuC/D at 30 days, suggesting they had differentiated into neurons. To test the hypothesis that social status and perception of an opportunity to rise in rank influenced cell proliferation, we compared numbers of BrdU-labeled cells in multiple brain nuclei among fish of different social status. Socially suppressed subordinate males had the lowest numbers of proliferating cells in all brain regions examined, but males that were given an opportunity to rise in status had higher cell proliferation rates within 1 day, suggesting rapid upregulation of brain mitotic activity associated with this social transition. Furthermore, socially isolated dominant males had similar numbers of BrdU-labeled cells compared with dominant males that were housed in a socially rich environment, suggesting that isolation has little effect on proliferation and that reduced proliferation in subordinates is a result of the social subordination. These results suggest that A. burtoni will be a useful model to analyze the mechanisms of socially induced neurogenesis in vertebrates. © 2012 Wiley Periodicals, Inc

Social descent with territory loss causes rapid behavioral, endocrine and transcriptional changes in the brain

In social species that form hierarchies where only dominant males reproduce, lower-ranking individuals may challenge higherranking ones, often resulting in changes in relative social status. How does a losing animal respond to loss of status? Here, using the African cichlid fish Astatotilapia burtoni, we manipulated the social environment, causing males to descend in rank, and then examined changes in behavior, circulating steroids and immediate early gene (IEG) expression (cfos, egr-1) in micro-dissected brain regions as a proxy for neuronal activation. In particular, we examined changes in the conserved \u27social behavior network\u27 (SBN), a collection of brain nuclei known to regulate social behaviors across vertebrates. Astatotilapia burtoni has rapidly reversible dominant-subordinate male phenotypes, so that within minutes, descending males lost their bright body coloration, switched to submissive behaviors and expressed higher plasma cortisol levels compared with non-descending and control males. Descending males had higher IEG expression throughout the SBN, but each brain region showed a distinct IEG-specific response in either cfos or egr-1 levels, but not both. Overall, SBN IEG patterns in descending males were distinctly different from the pattern observed in males ascending (subordinate to dominant) in social status. These results reveal that the SBN rapidly coordinates the perception of social cues about status that are of opposite valence, and translates them into appropriate phenotypic changes. This shows for the first time in a non-mammalian vertebrate that dropping in social rank rapidly activates specific socially relevant brain nuclei in a pattern that differs from when males rise to a higher status position. © 2013 Published by The Company of Biologists Ltd

The Value of Comparative Animal Research : Krogh’s Principle Facilitates Scientific Discoveries

There are no conflicts of interest to declare. This paper developed from the 2016 Early Career Impact Award from the Federation of Associations in Behavioral & Brain Sciences to TJS. TJS has received funding from The Leverhulme Trust. FJPE is in receipt of funding from the BBSRC (BB/M001555/1). The National Institutes of Health has funded RDF (NS 034950, NS093277, NIMH 087930), AGO (HD079573, IOS-1354760) and AMK (HD081959). BAA is an Arnold O. Beckman postdoctoral fellow.Peer reviewedPostprin