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

Abstract

Members of numerous animal species show consistent inter-individual differences in behaviours, but the forces generating animal “personality” or individuality remain unclear. We show that experiences gathered solely from social conflict can establish consistent differences in the decision of male crickets to approach or avoid a stimulus directed at one antenna. Adults isolated for 48 h from a colony already exhibit behavioural differences. Prior to staging a single dyadic contest, prospective winners approached the stimulus whereas prospective losers turned away, as they did also after fighting. In contrast, adults raised as nymphs with adult males present but isolated from them as last instar nymphs, all showed avoidance. Furthermore, adults raised without prior adult contact, showed no preferred directional response. However, following a single fight, winners from both these groups showed approach and losers avoidance, but this difference lasted only one day. In contrast, after 6 successive wins or defeats, the different directional responses of multiple winners and losers remained consistent for at least 6 days. Correlation analysis revealed examples of consistent inter-individual differences in the direction and magnitude of turning responses, which also correlated with individual aggressiveness and motility. Together our data reveal that social subjugation, or lack thereof, during post-embryonic and early adult development forges individuality and supports the notion of a proactive–reactive syndrome in crickets.

Developmental feedbacks and the emergence of individuality

“…diminishing returns) fitness landscapes give rise to negative behaviour-state feedbacks promoting behavioural convergence among individuals, while convex fitness landscapes give rise to positive feedbacks resulting in behavioural diversification among individuals. While it is clear from empirical studies that developmental processes are crucial in influencing the spread of within- and among-individual variation [24,25], our model produces novel results that implicate the specific shape of the selective environment in the adaptive developmental programs generating patterns of individual variation. That said, nonlinear fitness functions have previously been shown to have major effects on the development and evolution of a range of traits, including foraging behaviours [26], risk assessment and management [27,28], life-history transitions [29], the use of heuristics in decision making [30], and social behaviours [31,32].…”

Individual Scores for Associative Learning in a Differential Appetitive Olfactory Paradigm Using Binary Logistic Regression Analysis

“…This seems likely, considering that a similar situation has been reported for classical conditioning of honey bees, where the population comprises two types of animals, those that have acquired a conditioned response, and those that have not (Pamir et al, 2011 ). Furthermore, we have already demonstrated that crickets taken from standard breeding colonies show consistent inter-individual differences with respect to their general motility, exploratory behaviour, aggressiveness and their decision to approach or avoid a novel stimulus, resulting in basically two ethotypes comprising aggressive-proactive and submissive-reactive individuals (Rose et al, 2017 ; Balsam and Stevenson, 2020 , 2021 ). Notably, these differences appear to arise as a result of social experience, in particular social subjugation by aggressive adult males during development (Balsam and Stevenson, 2020 , 2021 ).…”

“…Furthermore, we have already demonstrated that crickets taken from standard breeding colonies show consistent inter-individual differences with respect to their general motility, exploratory behaviour, aggressiveness and their decision to approach or avoid a novel stimulus, resulting in basically two ethotypes comprising aggressive-proactive and submissive-reactive individuals (Rose et al, 2017 ; Balsam and Stevenson, 2020 , 2021 ). Notably, these differences appear to arise as a result of social experience, in particular social subjugation by aggressive adult males during development (Balsam and Stevenson, 2020 , 2021 ). Accordingly, we are currently testing the hypothesis, that aggressive social experience has a major impact on individual learning capacity.…”

“…In the present paper, therefore, we report individual learning scores for freely-moving male crickets, Gryllus bimaculatus . These insects have become a focus for studies of aggression (review: Stevenson and Rillich, 2019 ) and how experiencing aggression during development forges life-long inter-individual differences in adult behaviour (Rose et al, 2017 ; Balsam and Stevenson, 2020 , 2021 ). Earlier studies have also demonstrated the aptitude of crickets for studying learning and memory (review: Mizunami and Matsumoto, 2017 ).…”

Complex sexual-social environments produce high boldness and low aggression behavioral syndromes

“…For example, in the cavy (Cavia aperea), variation in birth season (associated with different stressors) leads to behavioral syndrome differences in adults (Guenther et al, 2014). In crickets, agonistic experience during development shapes individual differences in approach-avoidance behaviors, aggressiveness, and motility, which the authors argue supports a proactive and reactive coping style syndromes in that species (Balsam and Stevenson, 2021). The social environment can represent different levels of stress, and certainly variation in the type of mating interactions is likely to be a large source of stress variation.…”