Releasing stimuli and aggression in crickets: octopamine promotes escalation and maintenance but not initiation

Abstract

Biogenic amines have widespread effects on numerous behaviors, but their natural functions are often unclear. We investigated the role of octopamine (OA), the invertebrate analog of noradrenaline, on initiation and maintenance of aggression in male crickets of different social status. The key-releasing stimulus for aggression is antennal fencing between males, a behavior occurring naturally on initial contact. We show that mechanical antennal stimulation (AS) alone is sufficient to initiate an aggressive response (mandible threat display). The efficacy of AS as an aggression releasing stimulus was augmented in winners of a previous fight, but unaffected in losers. The efficacy of AS was not, however, influenced by OA receptor (OAR) agonists or antagonists, regardless of social status. Additional experiments indicate that the efficacy of AS is also not influenced by dopamine (DA) or serotonin (5HT). In addition to initiating an aggressive response, prior AS enhanced aggression exhibited in subsequent fights, whereby AS with a male antenna was now necessary, indicating a role for male contact pheromones. This priming effect of male-AS on subsequent aggression was dependent on OA since it was blocked by OAR-antagonists, and enhanced by OAR-agonists. Together our data reveal that neither OA, DA nor 5HT are required for initiating aggression in crickets, nor do these amines influence the efficacy of the natural releasing stimulus to initiate aggression. OA's natural function is restricted to promoting escalation and maintenance of aggression once initiated, and this can be invoked by numerous experiences, including prior contact with a male antenna as shown here.

Losing without Fighting - Simple Aversive Stimulation Induces Submissiveness Typical for Social Defeat via the Action of Nitric Oxide, but Only When Preceded by an Aggression Priming Stimulus

“…That the blockers had no clear effect on fights of otherwise non-stimulated crickets (Figure 4A) is not so surprising considering that amines are not essential for the initiation of aggression per se (Rillich and Stevenson, 2015). While the octopamine receptor blocker epinastine can lead to a just significant reduction of aggression in naïve crickets ( p < 0.05, see Stevenson et al, 2005; Rillich et al, 2011), this is not always evident (e.g., Rillich and Stevenson, 2011).…”

“…Rillich and Stevenson, 2015). Supporting this, the level and duration of aggression after AS only, was not significantly different to that for animals that received AS preceded by stimulation with a washed or female antenna.…”

David vs. Goliath: Serotonin modulates opponent perception between smaller and larger rivals

“…It is likely that particular 5-HT receptor subtypes contribute to the expression and inhibition of distinct aggressive behaviors as seen in Drosophila [16]. This mechanism could be extended further by the possibility of these receptors controlling the release of other neurochemicals known to increase aggression in insects such as octopamine [40,[43][44][45][46][47]. The underlying proximate mechanisms by which 5-HT modulates aggression as well as the correlation with other biochemical systems should be the focus of future studies.…”

Pre-adult aggression and its long-term behavioural consequences in crickets

“…Prior stimulation of an individual's antenna by manually stroking it with the freshly severed antenna of another adult donor male (priming) is known to increase aggression in adult males, particularly after losing a previous fight [26]. Here we compared how prior antennal Circles: median, boxes: interquartile range, whiskers: 10 th and 90 th percentiles.…”