Social Transitions Cause Rapid Behavioral and Neuroendocrine Changes

Abstract

In species that form dominance hierarchies, there are often opportunities for low-ranking individuals to challenge high-ranking ones, resulting in a rise or fall in social rank. How does an animal rapidly detect, process, and then respond to these social transitions? This article explores and summarizes how these social transitions can rapidly (within 24 h) impact an individual's behavior, physiology, and brain, using the African cichlid fish, Astatotilapia burtoni, as a model. Male A. burtoni form hierarchies in which a few brightly-colored dominant males defend territories and spawn with females, while the remaining males are subordinate, more drab-colored, do not hold a territory, and have minimal opportunities for reproduction. These social phenotypes are plastic and reversible, meaning that individual males may switch between dominant and subordinate status multiple times within a lifetime. When the social environment is manipulated to create males that either ascend (subordinate to dominant) or descend (dominant to subordinate) in rank, there are rapid changes in behavior, circulating hormones, and levels of gene expression in the brain that reflect the direction of transition. For example, within minutes, males ascending in status show bright coloration, a distinct eye-bar, increased dominance behaviors, activation of brain nuclei in the social behavior network, and higher levels of sex steroids in the plasma. Ascending males also show rapid changes in levels of neuropeptide and steroid receptors in the brain, as well as in the pituitary and testes. To further examine hormone-behavior relationships in this species during rapid social ascent, the present study also measured levels of testosterone, 11-ketotestosterone, estradiol, progestins, and cortisol in the plasma during the first week of social ascent and tested for correlations with behavior. Plasma levels of all steroids were rapidly increased at 30 min after social ascent, but were not correlated with behavior during the initial rise in rank, suggesting that behavior is dissociated from endocrine status. These changes during social ascent are then compared with our current knowledge about males descending in rank, who rapidly show faded coloration, decreased dominance behaviors, increased subordinate behaviors, and higher circulating levels of cortisol. Collectively, this work highlights how the perception of similar social cues that are opposite in value are rapidly translated into adaptive behavioral and neuroendocrine changes that promote survival and reproductive fitness. Finally, future directions are proposed to better understand the mechanisms that govern these rapid changes in social position.

Fig. 1

Male Astatotilapia burtoni rising in social rank rapidly produce both aggressive and reproductive behaviors within the first 30 min of social ascent. Within a few hours (6 h timepoint), aggressive behaviors decrease and reproductive behaviors increase. Sample sizes are N = 8–12 per timepoint.

Fig. 2

Circulating levels of steroid hormones are rapidly elevated at 30 min after subordinate male Astatotilapia burtoni are provided with an opportunity to rise in social rank. Despite their small testes and low gonadosomatic index (GSI), ascending males show higher levels of cortisol, estradiol, testosterone, 11-ketotestosterone (a fish-specific androgen), and progestins at 30 min after given a social opportunity compared with subordinate males. Dominant males also typically show higher levels in the plasma compared with subordinate males for all steroids measured. Data are plotted as mean ± SE for subordinate, 0.5, 6, 24, 72, and 120 h after social ascent, and dominant males. Sample sizes shown in parentheses indicate the number of individuals measured per timepoint. Different letters indicate statistical differences among groups at P ≤ 0.05.

Fig. 3

Rapid changes in mRNA levels of IEGs (egr-1/cfos) and sex steroid receptors in social-processing regions of the brain associated with Astatotilapia burtoni males rising in social rank. Relative size of the symbols in each schematic sagittal section of the brain indicates the relative mRNA levels of each gene between subordinate males (left) and males ascending in social rank at 30 min after ascent (right). Within each identified nucleus of the brain (gray ovals), only those genes that showed differences between subordinate and ascending males are shown. Note that the ascending phenotype has higher mRNA levels (i.e., more large symbols) of several types of steroid receptors within many regions of the brain compared with the subordinate phenotype. Locations of each nucleus within the fish brain are depicted to minimize overlap and are therefore only approximate. Rostral is to the left. ARα, ARβ, androgen receptor subtypes α and β; ATn, anterior tuberal nucleus; Dm, medial zone of the dorsal telencephalon; Dl, lateral zone of the dorsal telencephalon; ERα, ERβa, ERβb, estrogen receptor subtypes α, βa, and βb; Pit, pituitary; POA, preoptic area; Vs, supracommissural nucleus of the ventral telencephalon; VTn, ventral tuberal nucleus; Vv, ventral nucleus of the ventral telencephalon. Modified from Maruska et al. (2013b). (This figure is available in black and white in print and in color at Integrative and Comparative Biology online.)

Fig. 4

Summary of rapid phenotypic changes in Astatotilapia burtoni males that are ascending (A) or descending (B) in social rank. Changes that occur within the first 24 h of males rising or falling in rank are shown. These adaptive phenotypic changes occur on similar timescales, but are often opposite in valence. Compared with social ascent, less is known about rapid physiological and molecular changes during social descent, but some cellular changes and changes in level of gene expression along the brain–pituitary–testes axis occur more slowly (days to weeks) (White et al. 2002). Data are compiled from Parikh et al. (2006), Maruska and Fernald (2011a), Maruska et al. (2011), Kustan et al. (2012), Maruska et al. (2012, 2013a, 2013b), and Carpenter et al. (2014).

Fig. 5

Conceptual framework for transitions in social status. An individual’s phenotype is shaped by many inputs including genotype, body condition, reproductive state, and prior social experience. Animals living in social societies constantly evaluate the social environment by interacting with and watching other individuals in the population. Individuals of one phenotype (phenotype A) then integrate all of these inputs and make adaptive decisions on whether or not to transition to an alternative phenotype (phenotype B). This transition in social status is associated with many changes that can occur on a continuous timescale from rapid (seconds to hours) to slower (days to weeks). Examples of variables and traits most likely to occur on rapid timescales versus slower ones are indicated on the figure. These changes in phenotype take place on many biological levels (e.g., from whole-animal behavior to gene expression) and are often reversible, but may occur on different temporal scales depending on the direction of the transition (e.g., rising versus falling in social rank). Resulting phenotypes also have important consequences for survival and reproductive fitness. (This figure is available in black and white in print and in color at Integrative and Comparative Biology online.)