scholarly journals Plasticity of the Reproductive Axis Caused by Social Status Change in an African Cichlid Fish: II. Testicular Gene Expression and Spermatogenesis

Endocrinology ◽  
2011 ◽  
Vol 152 (1) ◽  
pp. 291-302 ◽  
Author(s):  
Karen P. Maruska ◽  
Russell D. Fernald

Abstract Reproduction in all vertebrates is controlled by the brain-pituitary-gonad (BPG) axis, which is regulated socially in males of the African cichlid fish Astatotilapia burtoni. Although social information influences GnRH1 neurons at the apex of the BPG axis, little is known about how the social environment and dominance affects the cellular and molecular composition of the testes to regulate reproductive capacity. We created an opportunity for reproductively suppressed males to ascend in status and then measured changes in gene expression and tissue morphology to discover how quickly the perception of this opportunity can influence the testes. Our results show rapid up-regulation of mRNA levels of FSH receptor and several steroid receptor subtypes in the testes during social ascent. In contrast, LH receptor was not elevated until 72 h after ascent, but this increase was coincident with elevated circulating androgens and early stages of spermatogenesis, suggesting a role in steroidogenesis. The spermatogenic potential of the testes, as measured by cellular composition, was also elevated before the overall increase in testes size. The presence of cysts at all stages of spermatogenesis, coupled with lower levels of gonadotropin and steroid receptors in subordinate males, suggests that the BPG axis and spermatogenesis are maintained at a subthreshold level in anticipation of the chance to gain a territory and become reproductively active. Our results show that the testis is stimulated extremely quickly after perception of social opportunity, presumably to allow suppressed males to rapidly achieve high reproductive success in a dynamic social environment.

Endocrinology ◽  
2011 ◽  
Vol 152 (1) ◽  
pp. 281-290 ◽  
Author(s):  
Karen P. Maruska ◽  
Berta Levavi-Sivan ◽  
Jakob Biran ◽  
Russell D. Fernald

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.


Author(s):  
Karen P. Maruska ◽  
Russell D. Fernald

How does an animal’s social environment shape its behavior and physiology, and what underlying molecular and genetic mechanisms lead to phenotypic changes? To address this question, the authors used a model system that exhibits socially regulated plastic phenotypes, behavioral complexity, molecular level access, and genomic resources. The African cichlid fishAstatotilapia burtoni, in which male status and reproductive physiology are under social control, has become an important model for studying the mechanisms that regulate complex social behaviors. This chapter reviews what is known about how information from the social environment produces changes in behavior, physiology, and gene expression profiles in the brain and reproductive axis ofA. burtoni. Understanding the mechanisms responsible for translating perception of social cues into molecular change in a model vertebrate is important for identifying selective pressures and evolutionary mechanisms that shape the brain and ultimately result in diverse and complex social behaviors.


2000 ◽  
Vol 347 (3) ◽  
pp. 643-651 ◽  
Author(s):  
Tore BENGTSSON ◽  
Barbara CANNON ◽  
Jan NEDERGAARD

In brown adipocytes, fundamental cellular processes (cell proliferation, differentiation and apoptosis) are regulated by adrenergic stimulation, notably through β-adrenergic receptors. The presence of all three β-receptor subtypes has been demonstrated in brown adipose tissue. Due to the significance of the action of these receptors and indications that the subtypes govern different processes, the adrenergic regulation of the expression of the β1-, β2- and β3-adrenoceptor genes was examined in murine brown-fat primary cell cultures. Moderate levels of β1-receptor mRNA, absence of β2-receptor mRNA and high levels of β3-receptor mRNA were observed in mature brown adipocytes (day 6 in culture). Noradrenaline (norepinephrine) addition led to diametrically opposite effects on β1- (markedly enhanced expression) and β3-gene expression (full cessation of expression, as previously shown). β2-Gene expression was induced by noradrenaline, but only transiently (< 1 h). The apparent affinities (EC50) of noradrenaline were clearly different (7 nM for the β1-gene and≤ 1 nM for the β3-gene), as were the mediation pathways (solely via β3-receptors and cAMP for the β1-gene and via β3-receptors and cAMP, as well as via α1-receptors and protein kinase C, for the β3-gene). The half-lives of the corresponding mRNA species were very short but different (17 min for β1-mRNA and 27 min for β3-mRNA), and these degradation rates were not affected by noradrenaline, implying that the mRNA levels were controlled by transcription. Inhibition of protein synthesis also led to diametrically opposite effects on β1- and β3-gene expression, but - notably - these effects were congruent with the noradrenaline effects, implying that a common factor regulating β1-gene expression negatively and β3-gene expression positively could be envisaged. In conclusion, very divergent effects of adrenergic stimulation on the expression of the different β-receptor genes were found within one cell type, and no unifying concept of adrenergic control of β-receptor gene expression can be formulated, either concerning different cell types, or concerning the different β-receptor subtype genes.


1999 ◽  
Vol 277 (1) ◽  
pp. R147-R153 ◽  
Author(s):  
Archana Chaudhry ◽  
James G. Granneman

Brown adipose tissue contains both β1- and β3-adrenergic receptors (β-ARs), and whereas both receptor subtypes can activate adenylyl cyclase, recent studies suggest that these subtypes have different pharmacological properties and may serve different signaling functions. In this study, primary brown adipocyte cultures were used to determine the role of β-AR subtypes in mediating lipolysis and uncoupling protein-1 (UCP1) gene expression, elicited by the physiological neurohormone norepinephrine (NE). NE increased both lipolysis and UCP1 mRNA levels in brown adipocyte cultures; the β1-receptor-selective antagonist CGP-20712A strongly antagonized the increase in UCP1 gene expression but had little effect on lipolysis. The β3-receptor-selective agonist CL-316243 (CL) also increased lipolysis and UCP1 mRNA levels, yet CL was more potent in stimulating lipolysis than UCP1 gene expression. NE also increased the phosphorylation of cAMP response element-binding protein (CREB) and perilipin (PL), both of which are protein kinase A substrates that are differentially targeted to the nucleus and lipid droplets, respectively. β1-receptor blockade inhibited NE-stimulated phosphorylation of CREB but not PL. The results suggest that β-AR subtypes regulate different physiological responses stimulated by NE in brown adipocyte cultures in part by differentially transducing signals to subcellular compartments.


Endocrinology ◽  
2006 ◽  
Vol 147 (11) ◽  
pp. 5119-5125 ◽  
Author(s):  
Brian C. Trainor ◽  
Hans A. Hofmann

Animals respond to environmental and social change with plasticity in the neural substrates underlying particular behavioral states. In the African cichlid fish Astatotilapia burtoni, social dominance status in males is accompanied by reduced somatic growth rate as well as increased somatostatin neuron size in the preoptic area. Although somatostatin is commonly studied within the context of growth, we show here for the first time that this ancient neuropeptide also plays a role in controlling social behavior. Somatostatin antagonists increased aggressive behavior in a dose-dependent fashion and the potent somatostatin agonist octreotide decreased aggression. We cloned and sequenced the genes encoding two somatostatin receptor subtypes in this species to study transcription in the gonads. When we examined somatostatin receptor gene expression in testes, expression of the somatostatin type 3 receptor was negatively correlated with an aggressive display and androgen levels. However, octreotide treatment did not reduce plasma testosterone or 11-ketotestosterone levels, suggesting that the behavioral effects of somatostatin are not mediated by androgens. These results show that somatostatin has important effects on social behavior. In dominant male A. burtoni, somatostatin may function to contain energetically costly processes such as somatic growth and aggressive behavior.


2020 ◽  
Vol 30 (1) ◽  
pp. 274-296
Author(s):  
Jelena Rajkov ◽  
Athimed El Taher ◽  
Astrid Böhne ◽  
Walter Salzburger ◽  
Bernd Egger

2017 ◽  
Vol 89 (3) ◽  
pp. 153-161 ◽  
Author(s):  
Chelsea A. Weitekamp ◽  
Tessa K. Solomon-Lane ◽  
Pamela Del Valle ◽  
Zegni Triki ◽  
Bridget M. Nugent ◽  
...  

Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni, to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.


Reproduction ◽  
2020 ◽  
Vol 159 (1) ◽  
pp. R31-R43
Author(s):  
María Florencia Scaia ◽  
Luciano Cavallino ◽  
Matías Pandolfi

Social animals with hierarchical dominance systems are susceptible to changes their environment. Interactions with conspecifics can greatly affect individual’s behavior and reproductive success. This review will show how social behavior modulates gonadal steroidogenesis and spermatogenesis in African and Neotropical cichlid fish with different social systems and how this modulation regulates reproductive capacity. Social behavior and aggressiveness are strongly linked to sex steroids, glucocorticoids and neuropeptides. The challenge hypothesis suggests that behavioral interactions increase androgen levels in response to social instability, but there is little evidence regarding estradiol levels. It has been recently demonstrated that in male Cichlasoma dimerus, a Neotropical cichlid fish, the challenge hypothesis could also be extended to estrogens. In C. dimerus, dominant males have higher gonadosomatic index than subordinated; the percentage of spermatocytes and spermatids is higher in subordinates, while dominants show a greater percentage of spermatozoa. In other species of African cichlids, socially suppressed subordinate males are not reproductively incompetent maintaining some activity at every level of their reproductive axis. Axis reactivation upon social ascent is similar to the initiation of puberty in mammals, as well as the reoccurrence of puberty observed in seasonally breeding animals. In conclusion, social behavior and reproductive strategies in females cichlids are still understudied, and Neotropical cichlids still constitute a group that deserves more attention, considering cichlids’ diversity in mating systems, reproductive behavior and parental care. This review highlights the importance of performing further studies and additional research in these two areas, which still remain to be addressed.


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