Rapid Behavioral and Genomic Responses to Social Opportunity

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.

Social status and sex independently influence androgen receptor expression in the eusocial naked mole-rat brain

“…The present data extend our observations to changes in gene and/or protein expression, as have been reported in statuschanging fish (Au et al, 2006;Burmeister et al, 2005Burmeister et al, , 2007. Based on available data, it is not possible to determine whether the relationship between AR and morphology is causal, or simply correlative.…”

Social control of brain morphology in a eusocial mammal

“…The behavioral and neural changes are reversible, as A. burtoni males may switch status both rapidly and repeatedly (46). Increases in immediateearly gene expression are observed in gonadotrophin-releasing hormone (GnRH) neurons within minutes of a relevant social stimulus, suggesting that this is a very early event in a molecular cascade presumably leading to longer-term changes (16). Breeding status is also reflected in altered neuropeptide expression in naked mole-rats, with subordinates exhibiting less vasopressin in the dorsomedial hypothalamus (19).…”

“…Similarly, breeding pairs maintain their status and continue to suppress reproduction of other colony members over long periods of time, even when not producing offspring and in the absence of gonads (53). Some effects of social status on the brain and behavior are also likely to be independent of the gonads in fish (16,54).…”

“…A change in status within a reproductive hierarchy alters neuronal gene expression, activity, and cell size in an African cichlid fish (11)(12)(13)(14)(15)(16). It is not known whether the transition from subordinate to breeder similarly affects the brains of naked mole-rats.…”

What can whole genome expression data tell us about the ecology and evolution of personality?

“…For example, a male cichlid that rises in social dominance and becomes territorial, which will give him the opportunity to court females and to breed, shows changes in gene expression in his brain in less than an hour after the change in dominance behaviour (Burmeister et al 2005). In such a case, behaviour is driving gene expression rather than vice versa.…”