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

Abstract

Social experience, particularly aggression, is considered a major determinant of consistent inter-individual behavioural differences between animals of the same species and sex. We investigated the influence of pre-adult aggressive experience on future behaviour in male, last instar nymphs of the cricket Gryllus bimaculatus. We found that aggressive interactions between male nymphs are far less fierce than for adults in terms of duration and escalation. This appears to reflect immaturity of the sensory apparatus for releasing aggression, rather than the motor system controlling it. First, a comparison of the behavioural responses of nymphs and adults to mechanical antennal stimulation using freshly excised, untreated and hexane-washed antennae taken from nymphs and adults, indicate that nymphs neither respond to nor produce sex-specific cuticular semiochemicals important for releasing aggressive behaviour in adults. Second, treatment with the octopamine agonist chlordimeform could at least partially compensate for this deficit. In further contrast to adults, which become hyper-aggressive after victory, but submissive after defeat, such winner and loser effects are not apparent in nymphs. Aggressive competition between nymphs thus appears to have no consequence for future behaviour in crickets. Male nymphs are often attacked by adult males, but not by adult females. Furthermore, observations of nymphs raised in the presence, or absence of adult males, revealed that social subjugation by adult males leads to reduced aggressiveness and depressed exploratory behaviour when the nymphs become adult. We conclude that social subjugation by adults during pre-adult development of nymphs is a major determinant of consistent inter-individual behavioural differences in adult crickets.

Agonistic experience during development establishes inter-individual differences in approach-avoidance behaviour of crickets

“…In response to the single touch stimulus, crickets tended to turn either towards it (positive turners) or away (negative turners). We never observed the aggressive mandible threat after the brief, single stimulus, which often occurs in response to repetitive stimulation 33 , 48 . However, positive turners ( n = 40 observed) occasionally lunged forward ( n = 9), exhibited body jerks ( n = 11) or generated the rival song ( n = 4), which was never shown by negative turners.…”

“…As for LTI w/ , they were taken from the colony on the day of the moult to the last nymphal stage and kept individually in social isolation until adult maturity. These animals thus only had contact to nymphs during development, which do not interact aggressively to generate winners and losers with long-term consequences for their subsequent behaviour 33 .…”

“…All focal animals engaged the hyper-aggressive opponents, but retreated after 1–15 s and subsequently avoided further contact with the opponent, which signalled victory by generating the rival song and chasing the focal animal. Thus, since the focal animal always lost these contests, we measured their individual aggressive motivation by recording the total duration of their interaction with the hyper-aggressive winner from initial antennal contact to retreat with a stopwatch to the nearest second 33 .…”

“…It was established later, however, that multiple intermittent defeats lead to practically life-long depression of agonistic behaviour in adult crickets 31 , 32 . Furthermore, adult crickets raised isolated from adult males throughout post-embryonic development, become more aggressive and motile than adults raised together with adult males 33 (see also for crayfish 34 , 35 and cockroaches 36 ). This suggests that differences in adult behaviour in crickets could arise from defeat stress during development, as shown in rodent models for human depression 37 , 38 , or alternatively as a more general consequence of deprivation of environmental stimulation during isolation 39 , 40 .…”

Long-Term Dietary Restriction Leads to Development of Alternative Fighting Strategies

“…A variety of studies on invertebrates showed that aggressive behavior is modulated by genetic factors (Dierick and Greenspan, 2006 ), environmental conditions (Rittschof and Robinson, 2013 ; Rillich et al, 2019 ), social influences (Kilgour et al, 2019 ; Balsam and Stevenson, 2020 ), sex (Benelli et al, 2015 ), and previous experiences (Goubault and Decuigniere, 2012 ; Rose et al, 2017 ). Indeed, previous victory and defeat induce behavioral plasticity in the form of winner and loser effects (previous victory/defeat increase the probability of winning/losing subsequent fight) (Hsu et al, 2006 ).…”