Abstract
Flaxseed oil is an excellent source of the essential omega-3 polyunsaturated fatty acid (PUFA) alpha-linolenic acid (ALA). Omega-3 PUFAs are important neuronal components and can counteract aggressive, depressive, and anxiety-like behavior, reduce glucocorticoid (e.g. cortisol) concentrations under chronic stress but also increase acute glucocorticoid responses. As glucocorticoids per se and glucocorticoid responsiveness can modulate the establishment of dominance hierarchies, we investigated if flaxseed oil high in ALA can promote social dominance through effects on glucocorticoid concentrations. Two male and two female groups of domestic guinea pigs (n = 9 per group) were maintained on a control or a 5% (w/w) flaxseed oil diet for four weeks. Social behaviors, hierarchy indices, locomotion, and saliva cortisol concentrations were determined during basal group housing conditions and stressful social confrontations with unfamiliar individuals of the other groups. Flaxseed groups had increased basal cortisol concentrations and showed no cortisol increase during social confrontations. Cortisol concentrations in control groups significantly increased during social confrontations. Such higher cortisol responses positively affected individual hierarchy indices in control males. However, flaxseed males became dominant irrespective of cortisol concentrations. In females, the opposite was detected, namely a higher dominant status in control compared to flaxseed females. Open-field- and dark-light-tests for anxiety-like behavior revealed no pronounced differences, but flaxseed males showed the highest locomotor activity. Flaxseed oil as an ALA source sex-specifically promoted social dominance irrespective of cortisol concentrations and responses. The underlying neuronal mechanisms remain to be determined, but a sex-specific energetic advantage may have accounted for this effect.
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Key Points
Social dominance has rarely been addressed with regard to the physiological and behavioral influences of dietary n-3 PUFAs. By modulating HPA-axis functions, glucocorticoid concentrations, and social behavior, n-3 PUFAs may ultimately affect social dominance. We therefore investigated the effects of flaxseed oil high in ALA on cortisol concentrations, social behavior, social dominance, locomotion, and anxiety-like behavior in male and female domestic guinea pigs. Here it was hypothesized that flaxseed oil supplementation results in a stronger cortisol increase during social confrontations, thereby promoting social dominance, but counteracts anxiety-like behavior. Effects on social dominance were mainly expected in males due to stronger pronounced social hierarchies compared to females.
The results presented here suggest sex-specific positive effects of cortisol responses and of flaxseed oil high in n-3 PUFAs on social dominance. Corresponding to these effects, saliva cortisol responses were inversely related to basal cortisol concentrations and positively affected individual hierarchy indices during social confrontations in control males. Importantly, however, a sex-specific contribution of flaxseed oil to social dominance was independent of cortisol concentrations and responsiveness but apparently hindered control males from becoming dominant. In contrast, a negative effect of flaxseed oil supplementation was detected in females, finally resulting in a subdominant status. Anxiety-like behaviors in the open-field and dark-light tests determined by the time spent in the center and the shelter, respectively, were not affected by flaxseed oil supplementation. Nevertheless, a higher locomotor activity in flaxseed males throughout and differences in the social organization could explain the detected effects on cortisol concentrations and, furthermore, the sex-specific dominance outcomes during social confrontations.
Analysis of social behaviors during group housing revealed no differences between diet groups, which could have explained the increased cortisol concentrations in flaxseed groups. Generally higher basal cortisol concentrations in males compared to females were presumably related to more aggressive and dominance behavior in order to maintain social hierarchies. Social dominance of flaxseed males was not based on aggressive behavior but on their assertiveness, as reflected in increased dominance behavior. In contrast, the final dominant status of control females was indeed related to increased aggressiveness, which could have also been facilitated by their cortisol responses.
In addition to a sex-specific effect of flaxseed oil on social dominance, flaxseed males showed highest locomotor activity throughout the study.
The group housing situation further revealed a negative relationship between cortisol concentrations and hierarchy indices in control groups, while no such effect was detected in flaxseed groups. Increased basal cortisol concentrations in flaxseed groups are therefore mainly attributable to more dominant individuals.
This study provides evidence that flaxseed oil high in ALA sex-specifically promotes social dominance irrespective of cortisol concentrations and responsiveness, whereby a possible energetic advantage in males may have accounted for this effect. These sex differences require closer examination in order to unravel the role of n-3 PUFAs and glucocorticoids in modulating social behavior and social hierarchies.