Abstract
From primates to bees, social status regulates reproduction. In the cichlid fish Astatotilapia (Haplochromis) burtoni, subordinate males have reduced fertility and must become dominant to reproduce. This increase in sexual capacity is orchestrated by neurons in the preoptic area, which enlarge in response to dominance and increase expression of gonadotropin-releasing hormone 1 (GnRH1), a peptide critical for reproduction. Using a novel behavioral paradigm, we show for the first time that subordinate males can become dominant within minutes of an opportunity to do so, displaying dramatic changes in body coloration and behavior. We also found that social opportunity induced expression of the immediate-early gene egr-1 in the anterior preoptic area, peaking in regions with high densities of GnRH1 neurons, and not in brain regions that express the related peptides GnRH2 and GnRH3. This genomic response did not occur in stable subordinate or stable dominant males even though stable dominants, like ascending males, displayed dominance behaviors. Moreover, egr-1 in the optic tectum and the cerebellum was similarly induced in all experimental groups, showing that egr-1 induction in the anterior preoptic area of ascending males was specific to this brain region. Because egr-1 codes for a transcription factor important in neural plasticity, induction of egr-1 in the anterior preoptic area by social opportunity could be an early trigger in the molecular cascade that culminates in enhanced fertility and other long-term physiological changes associated with dominance.
Highlights
IntroductionDominance can have long-term physiological consequences. For example, dominance status has been shown to control fertility [1,2,3], neurogenesis [4], growth rate [5], and stress physiology [6,7]
Among social animals, dominance can have long-term physiological consequences
What is the behavioral response to perception of social opportunity? Second, what is the genomic response to social opportunity in the anterior parvocellular preoptic nucleus (aPPn) and how does this relate to gonadotropin-releasing hormone 1 (GnRH1) neurons? To answer these questions, we developed a novel behavioral paradigm in which resident subordinate males were provided an opportunity to ascend in status in their familiar home environments
Summary
Dominance can have long-term physiological consequences. For example, dominance status has been shown to control fertility [1,2,3], neurogenesis [4], growth rate [5], and stress physiology [6,7]. Subordinate males have smaller, lessmature testes [3]; they lack a territory with a spawning site; they do not display the body coloration advertising dominance; and they infrequently perform dominance behaviors, such as territorial defense and courtship Among vertebrates, such differences in reproductive maturation are controlled primarily by the hypophysiotropic gonadotropin-releasing hormone (GnRH) neurons in the basal forebrain [8]. The GnRH1 neurons in the aPPn have larger somas [9,10], higher GnRH1 gene expression [11], and altered electrical properties [12] compared to subordinates These differences in GnRH1 neurons are controlled by social status [10,13] and presumably underlie the differences in testes size. Other forms of GnRH, GnRH2 and GnRH3, are expressed in the midbrain tegmentum and the terminal nerve ganglion, respectively, but they do not appear to regulate reproductive physiology in this species [11,14,15], nor do they demonstrate socially induced neural plasticity in soma size or gene expression [11], GnRH2 has been implicated in regulating reproduction in mammals [16]
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