Social regulation of male reproductive plasticity in an African cichlid fish

Abstract

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's 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 (brain-pituitary-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.

Fig. 1

Summary of socially-mediated differences in the BPG axis between stable subordinate and stable dominant male phenotypes of Astatotilapia burtoni. Dominant males (right) have an up-regulated BPG axis, defend territories, and regularly court and spawn with females, whereas subordinate males (left) have a suppressed BPG axis, do not hold territories, and typically do not reproduce. All of these features are influenced by the social environment and can rapidly change (minutes to days) when males are given a social opportunity to ascend, or rise, to a higher-ranking status. Only those measures directly relevant to the BPG axis are shown. Red GnRH1 neurons represent immunohistochemical staining in the preoptic area of the brain, and GnRH-R1 staining (black label; with purple cresyl violet counterstain) in the pituitary gland is from an in situ hybridization experiment. Italicized genes indicate mRNA levels measured via qPCR. Cross sections of testes were stained with hemotoxylin and eosin. Modified in part from Maruska and Fernald (2011b) and Maruska et al. (2013), and information was compiled from a number of studies (Davis and Fernald 1990; Chen and Fernald 2006; Maruska and Fernald 2010a, 2011a; Maruska et al. 2011; Huffman et al. 2012). ↑, higher relative levels; ↓, lower relative levels. ARα, ARβ, androgen receptor subtypes α and β; ERα, estrogen receptor subtype α; FSHβ, β-subunit of follicle stimulating hormone; FSHR, FSH receptor; GnRH1, gonadotropin releasing hormone 1; GnRH-R1, GnRH receptor subtype 1; GR1a, GR1b, GR2, glucocorticoid receptor subtypes 1a, 1b, 2; GSI, gonadosomatic index; LHβ, β-subunit of luteinizing hormone; LHR, LH receptor; MR, mineralocorticoid receptor; StAR, steroidogenic acute regulatory protein.

Fig. 2

Social opportunity rapidly activates the brain in male A. burtoni rising in status. (A) Social opportunity rapidly increases mRNA levels of the IEG cfos in brain nuclei involved in processing social information. Relative mRNA levels (normalized to the reference genes 18s and g3pdh) measured via qPCR in microdissected regions of the brain were higher in males that ascended in social status 30 min prior compared with either stable subordinate or stable dominant control males (Maruska et al. 2013). ATn, anterior tuberal nucleus; Ce, cerebellum; Dm, medial part of the dorsal telencephalon; Dl, lateral part of the dorsal telencephalon; Pit, pituitary; POA, preoptic area; Vs, supracommissural nucleus of the ventral telencephalon; VTn, ventral tuberal nucleus; Vv, ventral nucleus of the ventral telencephalon. (B) The IEG egr-1 (small black dots detected via in situ hybridization) is rapidly up-regulated in GnRH1 neurons (arrows) of the preoptic area within 20 min of a male rising in social rank (Burmeister et al. 2005). (C) Stable dominant males have larger GnRH1 neurons compared with stable subordinate males, but an increase in soma size is detected just 24 h after males ascended in social status. (D) GnRH1 mRNA levels measured in whole brains via qPCR are higher in newly ascended males at 30 min after social opportunity compared with stable subordinate males, but still lower than that of stable dominant males. (E) Cell proliferation, quantified by BrdU labeling, in the preoptic area (POA) is relatively low in stable subordinate males, but has increased in males at 24 h after they rise in social rank (Maruska et al. 2012a). Sample sizes represent the number of animals used for each experiment and are indicated in parentheses. Bars with different letters indicate significant differences at P < 0.05.