Mechanisms of experience dependent control of aggression in crickets
Introduction
Various behavioural theories predict that animals gather information from ritualized agonistic signals exchanged during fighting to assess their win chances, which depend on physical disparities (size, strength, weaponry) as well as on ‘aggressive motivation’ — a product of the effects of experiences such as the presence of resources, their value, outcome of previous fights and social upbringing [1, 2•]. But what are the proximate mechanisms? How do such diverse experiences determine aggressive motivation, and how is this represented in the nervous system? How do animals ‘assess’ agonistic signals and how do they affect aggression? Just how exactly do animals seem to know when best to fight or flee? We summarize recent insights from studies on male field crickets (Gryllus bimaculatus).
But why crickets? For one, their miniature brains contain comparatively few, individually identifiable neurons, but nonetheless have the capacity to generate sophisticated social interactions [3]. Furthermore, their impressive fighting behaviour is highly ritualized [4] and influenced by a wealth of experiences including physical exertion [5], winning [6••], losing [7], the presence of shelter [8••], food [9] or females [10], courtship and mating [11, 12•], their song [13, 14•, 15•], social isolation and crowding (PA Stevenson, J Rillich, Isolation induced aggression in crickets is a result of recovery from social subjugation). In some quarters, there is a growing tendency to attribute insects with experiencing conscious emotions (see [17•] for a rational commentary). We do not specifically address this, its hard to prove and impossible to refute. Even so, the experimental data illustrate that crickets can equate potential costs and benefits of aggression to generate adaptive aggressive behaviour, quite simply, by exploiting the basic principles of neuromodulation, without necessitating rational, conscious emotions or reason, and this is perhaps their greatest advantage.
Section snippets
Initiation of fighting in crickets
When two cricket meets, they fence with their antennae, which are active tactile and olfactory sensors [18]. This behaviour is sufficient and necessary for eliciting aggressive responses (mandible spreading, aggressive song production, fighting), and males with ablated antennae court [19]. Pheromonal signatures signal a cricket's species and sex [20], and a pheromone promoting aggression has been identified in male fruit flies [21••]. The antennal afferent pathways in the cricket brain are
Aggression and biogenic amines
Every single synaptic connection is potentially subject to modulation by biogenic amines [29•], hence their powerful influences on behaviour. In mammals, the adrenergic/noradrenergic system is generally associated with the fight or flee response, but no consistent relationship with aggression has been found, with most studies focusing on serotonin [30••], perhaps due to its suppressive effects. In insects and other protostomes adrenaline/noradrenaline is replaced by the analogous amine
Physical exertion and aggression — the flight effect
In insects, chronic stress, physical exertion, and particularly flying activate specific sets of octopaminergic neurones (DUM/VUM-cells [41]), and lead to a surge of octopamine in the haemolymph [4, 42]. Flying also induces a pronounced, transient increase in the aggressiveness of crickets lasting some 15–30 min [5]. This effect depends on activation of the octopaminergic system. It is reproduced by treatment with the octopamine agonist chlordimeform, prohibited by inhibiting octopamine
Effects of fighting and winning
In many species, winning a conflict makes an individual more aggressive and more likely to win subsequent encounters [46•]. In mammals, winner effects are mostly long lasting, and involve increased androgen receptor expression in the brain [47••]. A shorter winner effect (<20 min) is also evident in crickets [6••, 7, 48] and this is selectively blocked by octopamine receptor antagonists [6••]. The physical exertion of fighting, which leads to a 5 fold increase in octopamine haemolymph levels [49
Resources and the residency effect
Irrespective of species, holders of key resources are more likely to win disputes, but it is unclear how this is controlled [46•]. In crickets, burrows are valuable assets, offering shelter and attracting females, and their owners zealously fight off intruding males [52, 53]. In a phylogenetic context, cricket species with burrowing males are more aggressive than species with non-burrowing males [54]. In the laboratory, initially submissive crickets become highly aggressive after occupying an
Octopamine and reward
The paradoxical question is how experiences as diverse as flying, winning and residency, each lead to enhanced aggressiveness via a common mechanism? In mammals, physical exertion [55], aggressive encounters and winning each induce changes in activity and functioning of brain regions that mediate motivation and reward [56••] and we have proposed an analogous scenario for crickets [57]. The concept of reward in insects is derived from studies of appetitive learning [58••, 59••]. In a now
Isolation, crowding and aggression
In insects, social isolation and crowding produce dramatic behavioural changes, and some are regulated by biogenic amines [64] (SJ Simpson, PA Stevenson, Neuromodulation of social behaviour in insects. In Oxford Handbook of Molecular Psychology. Oxford University Press, 2013, unpublished data). Regarding aggression, this is generally reduced in grouped animals, and heightened in social isolates [46•]. In fruit flies, reduced aggression of socially grouped males is mediated in part by activation
Conclusions
The ‘decision to fight or flee’ in crickets could be accounted for by simply modulating their relative behavioural thresholds in response to potentially rewarding and aversive experiences (Figure 1). Winning, resources, fighting and flying promote the tendency to fight by activating the octopaminergic reward pathway. Octopamine can thus be considered as setting the motivational level of aggression. Agonistic actions of the opponent, in contrast, have some negative aversive quality, that promote
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
The authors gratefully acknowledge the contributions of our co-authors to the original work, in particularly Jan Rillich. Support by the German Research Council (DFG) is gratefully acknowledged (Research Group 1363, STE 714/4-1).
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