Role of cAMP signalling in winner and loser effects in crayfish agonistic encounters

Abstract

For territorial animals, establishment of status-dependent dominance order is essential to maintain social stability. In agonistic encounters of the crayfish Procambarus clarkii, a difference of body length of 3-7% is enough for larger animals to become dominant. Despite a physical disadvantage, small winners of the first pairings were more likely to win subsequent conflicts with larger inexperienced animals. In contrast, the losers of the first pairings rarely won subsequent conflicts with smaller naive animals. Such experiences of previous winning or losing affected agonistic outcomes for a long period. The winner effects lasted more than 2 weeks and the loser effect lasted about 10 days. Injection of 5HT1 receptor antagonist into the dominant animals 15-30 min after establishment of dominance order blocked the formation of the winner effects. In contrast, injection of adrenergic-like octopamine receptor antagonist into subordinate animals blocked the formation of the loser. 5HT1 receptors are negatively coupled to adenylyl cyclase and adrenergic-like octopamine receptors are positively coupled. Consistent with this, dominant animals failed to show the winner effect when injected with pCPT-cAMP, a cAMP analogue, and subordinate animals failed to show a loser effect when injected with adenylyl cyclase inhibitor SQ 22536. These results suggest that an increase and decrease of cAMP concentration is essential in mediating loser and winner effects, respectively. Furthermore, formation of the loser effect was blocked by injection of protein kinase A (PKA) inhibitor H89, suggesting long-term memory of the loser effect is dependent on the cAMP-PKA signalling pathway.

The effects of quality of shelters and prior residence on Marmorkrebs (marbled crayfish)

“…This result is similar to a winner effect that winning small animals in previous fights tend to win against large animals in the subsequent fights (Momohara et al, 2013). A decrease in cAMP level in the brain mediated by serotonin induces the winner effect (Momohara et al, 2015(Momohara et al, , 2016. At the moment, the neurochemical and physiological bases underlying the residence effect are unclear, but certain biogenic amines like serotonin could underlie this effect.…”

“…Marmorkrebs are thought to be a parthenogenetic form of Procambarus fallax (Scholtz et al, 2003;Martin et al, 2007) and/or Procambarus virginalis (Vogt et al, 2015). They produce genetically uniform clones and their central nervous system is probably similar to that of Procambarus clarkii (Faulkes, 2016), in which agonistic interactions and winner/loser effects have been well studied (Fujimoto et al, 2011;Sato and Nagayama, 2012;Momohara et al, 2016Momohara et al, , 2018Araki et al, 2013). Their behavioural plasticity and its neurochemical basis are well characterized (Kasuya and Nagayama, 2016;Shiratori et al, 2017).…”

Cyclic AMP‐regulated opposing and parallel effects of serotonin and dopamine on phototaxis in the Marmorkrebs (marbled crayfish)

“…They also affect neural activity underlying learning and memory (Hammer & Menzel, ; Kandel, ; Schwaerzel et al ., ; Araki et al ., ; Menses & Liy‐Salmeron, ). Previous research has also characterized the effects of biogenic amines downstream of their signalling pathways (Araki et al ., ; Araki & Nagayama, ; Kandel, ; Nagayama & Araki, ; Momohara et al ., ). Serotonin and dopamine contribute to thermotaxic memory behaviour in C. elegans (Li et al ., ).…”

Social experience alters different types of learning abilities controlled by distinct brain nuclei inKryptolebias marmoratus

“…Winner and loser effects were originally defined by changes in aggression after agonistic interactions, and thus most previous research focused on the roles of androgenic hormones and associated receptors in mediating these effects. However, recent studies in invertebrates have revealed that learning and memory may also change in predictable ways with winning and losing experience (21,31,32). For instance, fruit flies (Drosophila melanogaster) can recognize conspecifics, and losers behave differently when encountering familiar versus unfamiliar opponents, suggesting that learning and memory accompany changes in social status (31).…”