Department of Biology, Stanford University, 371 Serra Mall, Stanford, CA 94305, USA.
J Exp Biol. 2013 Oct 1;216(Pt 19):3656-66. doi: 10.1242/jeb.088617. Epub 2013 Jun 20.
In social species that form hierarchies where only dominant males reproduce, lower-ranking individuals may challenge higher-ranking 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 'social behavior network' (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.
在形成只有支配雄性繁殖的等级制度的社会物种中，低等级个体可能会挑战高等级个体，这通常会导致相对社会地位的变化。失去地位的动物会如何反应？在这里，我们使用非洲丽鱼科鱼类 Astatotilapia burtoni 操纵社会环境，导致雄性等级下降，然后检查行为、循环类固醇和即时早期基因 (IEG) 表达（cfos、egr-1）在微解剖大脑区域中的变化，作为神经元激活的替代物。特别是，我们检查了保守的“社会行为网络”（SBN）的变化，该网络是一组已知在整个脊椎动物中调节社会行为的脑核。Astatotilapia burtoni 具有快速可逆的支配-从属雄性表型，因此在几分钟内，下降的雄性会失去鲜艳的体色，转而表现出顺从的行为，并表现出比非下降和对照雄性更高的血浆皮质醇水平。下降的雄性在整个 SBN 中都有更高的 IEG 表达，但每个大脑区域的 cfos 或 egr-1 水平都表现出不同的 IEG 特异性反应，而不是两者都有。总体而言，下降雄性的 SBN IEG 模式与在社会地位上升（从从属到支配）的雄性中观察到的模式明显不同。这些结果表明，SBN 迅速协调了对地位的社会线索的感知，这些线索具有相反的效价，并将其转化为适当的表型变化。这首次表明，在非哺乳动物脊椎动物中，社会等级下降会迅速激活与特定社会相关的大脑核，其模式与雄性上升到更高地位时不同。
