Abstract
Theoretical and empirical studies have sought to explain the formation and maintenance of social relationships within groups. The resulting dominance hierarchies have significant fitness and survival consequences dependent upon social status. We hypothesised that each position or rank within a group has a distinctive brain gene expression profile that correlates with behavioural phenotype. Furthermore, transitions in rank position should determine which genes shift in expression concurrent with the new dominance status. We used a custom cDNA microarray to profile brain transcript expression in a model species, the rainbow trout, which forms tractable linear hierarchies. Dominant, subdominant and submissive individuals had distinctive transcript profiles with 110 gene probes identified using conservative statistical analyses. By removing the dominant, we characterised the changes in transcript expression in sub-dominant individuals that became dominant demonstrating that the molecular transition occurred within 48 hours. A strong, novel candidate gene, ependymin, which was highly expressed in both the transcript and protein in subdominants relative to dominants, was tested further. Using antibody injection to inactivate ependymin in pairs of dominant and subdominant zebrafish, the subdominant fish exhibited a substantial increase in aggression in parallel with an enhanced competitive ability. This is the first study to characterise the molecular signatures of dominance status within groups and the first to implicate ependymin in control of aggressive behaviour. It also provides evidence for indirect genetic effect models in which genotype/phenotype of an individual is influenced by conspecific interactions within a group. The variation in the molecular profile of each individual within a group may offer a new explanation of intraspecific variation in gene expression within undefined groups of animals and provides new candidates for empirical study.
Highlights
Individual fitness is driven by the acquisition of key resources necessary for survival and reproduction
1762 ESTs were annotated by homology alignment, representing 494 unique genes identified by BLASTx searching of which 454 possessed Gene Ontology annotation
For the N/S comparison the differences were nonexistent at 2 h, but increased by 48 h until they broadly matched that expected for the D/S contrast. Together these results demonstrate that the differentially expressed genes identified from the stable hierarchies displayed the expected transitions when sub-dominant fish assumed a dominant status, and that the main changes in transcript expression occurred between the 2 h and 48 h time points after manipulation
Summary
Individual fitness is driven by the acquisition of key resources necessary for survival and reproduction. Social status often plays a crucial role in gaining these resources, with dominant animals monopolising or having priority access, and rank within a social group having a profound effect upon reproductive success, survival and fitness [1]. Dominant individuals are more willing to perform aggressive attacks [2,3,4,5] They have lower stress hormone levels, differing brain serotonergic activity, more efficient metabolic and growth rates than those measured in subdominant and subordinate animals [6]. These parameters are determined sometime after a dominance hierarchy has been established and, it has been difficult to separate cause and consequence. A mechanistic approach may identify indirect genetic effects such as phenotypic traits of conspecifics that contribute to individual fitness to explain the evolution of complex social groups [7]
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