Plasticity of the reproductive axis caused by social status change in an african cichlid fish: I. Pituitary gonadotropins

Abstract

Social position in a dominance hierarchy is often tightly coupled with fertility. Consequently, an animal that can recognize and rapidly take advantage of an opportunity to rise in rank will have a reproductive advantage. Reproduction in all vertebrates is controlled by the brain-pituitary-gonad axis, and in males of the African cichlid fish Astatotilapia burtoni, GnRH1 neurons at the apex of this axis are under social control. However, little is known about how quickly social information is transformed into functional reproductive change, or about how socially controlled changes in GnRH1 neurons influence downstream actions of the brain-pituitary-gonad axis. We created an opportunity for reproductively suppressed males to ascend in status and then measured how quickly the perception of this opportunity caused changes in mRNA and protein levels of the pituitary gonadotropins. mRNA levels of the β-subunits of LH and FSH rose rapidly in the pituitary 30 min after suppressed males perceived an opportunity to ascend. In contrast, mRNA levels of GnRH receptor-1 remained unchanged during social transition but were higher in stable dominant compared with subordinate males. In the circulation, levels of both LH and FSH were also quickly elevated. There was a positive correlation between mRNA in the pituitary and circulating protein levels for LH and FSH, and both gonadotropins were positively correlated with plasma 11-ketotestosterone. Our results show that the pituitary is stimulated extremely rapidly after perception of social opportunity, probably to allow suppressed males to quickly achieve reproductive success in a dynamic social environment.

Figure 1

Levels of LHβ, FSHβ, and GnRH-R1 mRNA in the pituitary of male African cichlid fish A. burtoni during social ascent. A, Levels of LHβ (bars) were rapidly elevated above stable subordinate levels at 30 min after perception of social opportunity and further increased to reach stable dominant levels by 72 h. Serum 11-KT levels (•) (data from Ref. 17) showed a similar pattern of increase at 30 min, were relatively stable through 24 h, and then further increased to stable dominant levels by 72 h. B, Levels of FSHβ were also rapidly elevated at 30 min after ascent and reached a maximum at 120 h after perception of social opportunity. C, GnRH-R1 levels did not change during social transition but were approximately 2-fold higher in stable dominant males compared with stable subordinates. Data are plotted as relative mRNA levels (mean ± se) referenced to the geometric mean of two housekeeping genes (18s and G3PDH). Bars with different letters represent significant differences (P < 0.05), and sample sizes are indicated within each bar on the bottom graph.

Figure 2

Circulating plasma levels of LH and FSH in male A. burtoni during social ascent. Plasma levels of both LH and FSH were 2-fold higher in stable dominant males compared with stable subordinate males. Furthermore, LH and FSH were rapidly elevated at 30 min after a suppressed subordinate male was given an opportunity to ascend in social status. Data are plotted as mean ± se. Bars with different letters represent significant differences (P < 0.05), and sample sizes are indicated within each bar on the bottom graph.

Figure 3

Pituitary gonadotropin mRNA levels are correlated with circulating plasma concentrations in male A. burtoni. There was a positive correlation between pituitary mRNA levels of LHβ and FSHβ and circulating plasma levels of LH and FSH. Transcript expression is plotted as relative mRNA levels referenced to the geometric mean of two housekeeping genes (18s and G3PDH). Correlation coefficients (r) and P values are shown.

Figure 4

GSI is correlated with pituitary mRNA and circulating plasma levels of LH and FSH in male A. burtoni. GSI was positively correlated with both circulating LH and FSH and pituitary mRNA levels of LHβ and FSHβ. Correlation coefficients (r) and P values are shown.

Figure 5

Summary of physiological changes in the pituitary and circulation during social ascent in male A. burtoni. Coincident physiological elevations occur rapidly at 30 min after social opportunity in both the pituitary and the circulation, followed by further increases at later time points to reach stable dominant male levels. Data are expressed as arbitrary values to illustrate overall patterns of temporal changes among measures. 11-KT data are from Ref. .