Differential Gene Expression Correlates with Behavioural Polymorphism during Collective Behaviour in Cockroaches.

Consistent inter-individual variation in the propensity to perform different tasks (animal personality) can contribute significantly to the success of group-living organisms. The distribution of different personalities in a group influences collective actions and therefore how these organisms interact with their environment. However, we have little understanding of the proximate mechanisms underlying animal personality in animal groups, and research on this theme has often been biased towards organisms with advanced social systems. The goal of this study is to investigate the mechanistic basis for personality variation during collective behaviour in a species with rudimentary societies: the American cockroach. We thus use an approach which combines experimental classification of individuals into behavioural phenotypes ('bold' and 'shy' individuals) with comparative gene expression. Our analyses reveal differences in gene expression between behavioural phenotypes and suggest that social context may modulate gene expression related to bold/shy characteristics. We also discuss how cockroaches could be a valuable model for the study of genetic mechanisms underlying the early steps in the evolution of social behaviour and social complexity. This study provides a first step towards a better understanding of the molecular mechanisms associated with differences in boldness and behavioural plasticity in these organisms.

Variation in personality can substitute for social feedback in coordinated animal movements.

Collective movements are essential for the effective function of animal societies, but are complicated by the need for consensus among group members. Consensus is typically assumed to arise via feedback mechanisms, but this ignores inter-individual variation in behavioural tendency ('personality'), which is known to underpin the successful function of many complex societies. In this study, we use a theoretical approach to examine the relative importance of personality and feedback in the emergence of collective movement decisions in animal groups. Our results show that variation in personality dramatically influences collective decisions and can partially or completely replace feedback depending on the directionality of relationships among individuals. The influence of personality increases with the exaggeration of differences among individuals. While it is likely that both feedback and personality interact in nature, our findings highlight the potential importance of personality in driving collective processes.

Personality variation improves collective decision-making in cockroaches.

Many animals live in groups and engage in collective actions which can enhance their fitness. One common example is collective decision-making, which mainly arises from social interactions that modify the individual behaviour. Despite the widespread interest in animal personalities on the one hand and in social effects (such as social organisation, social learning or anti-predator behaviour) on the other, the question of how the amount of among-individual differences, coupled with social interactions, influence group cohesion has rarely been addressed. For this purpose, I used a modelling approach based on aggregation behaviour of cockroaches to explore the mechanisms underlying such context-dependent behaviour. The results of simulations considering different degrees (none, medium, high) of personality variation in a non-social and social context were compared to experimental patterns of aggregation dynamics in cockroaches. The comparison between the simulated and experimental data show that only a model that considers differences in individuals was able to reproduce the experimental patterns of individuals and groups. In addition, the comparison between models suggest that some individuals may play a keystone role during aggregation dynamics, influencing the behaviour of others and facilitating the collective decision. Finally, I show that personality variation amplifies the effects of social inter-attractions, thus increasing the speed of aggregation, shedding light on the mechanisms underpinning social modification of individual behaviour.

Measuring affect-related cognitive bias: Do mice in opposite affective states react differently to negative and positive stimuli?

Affect-driven cognitive biases can be used as an indicator of affective (emotional) state. Since humans in negative affective states demonstrate greater responses to negatively-valenced stimuli, we investigated putative affect-related bias in mice by monitoring their response to unexpected, task-irrelevant stimuli of different valence. Thirty-one C57BL/6J and 31 DBA/2J females were individually trained to return to their home-cage in a runway. Mice then underwent an affective manipulation acutely inducing a negative (NegAff) or a comparatively less negative (CompLessNeg) affective state before immediately being tested in the runway with either an 'attractive' (familiar food) or 'threatening' (flashing light) stimulus. Mice were subsequently trained and tested again (same affective manipulation) with the alternative stimulus. As predicted, mice were slower to approach the light and spent more time with the food. DBA/2J mice were slower than C57BL/6J overall. Contrary to predictions, NegAff mice tended to approach both stimuli more readily than CompLessNeg mice, especially the light, and even more so for DBA/2Js. Although the stimuli successfully differentiated the response of mice to unexpected, task-irrelevant stimuli, further refinement may be required to disentangle the effects of affect manipulation and arousal on the response to valenced stimuli. The results also highlight the significant importance of considering strain differences when developing cognitive tasks.

Conflictual influence of humidity during shelter selection of the American cockroach (Periplaneta americana).

In collective decision-making, when confronted with different options, groups usually show a more marked preference for one of the options than do isolated individuals. This results from the amplification of individual preferences by social interactions within the group. We show, in an unusual counter-example, that when facing a binary choice between shelters with different relative humidities, isolated cockroaches of the species Periplaneta americana select the wettest shelter, while groups select the driest one. This inversion of selection results from a conflictual influence of humidity on the probabilities of entering and leaving each shelter. It is shown that the individual probability of entering the wettest shelter is higher than the group probability and is increased by previous entries and exits. The probability of leaving each shelter decreases in the population due to social interactions, but this decrease is less pronounced in the wettest shelter, suggesting weaker social interactions. A theoretical model is developed and highlights the existence of tipping points dependent on population size, beyond which an inversion of selection of a resting place is observed.

The role of personality variation, plasticity and social facilitation in cockroach aggregation.

Personality variation has been proven to affect ecology, evolution and group behaviour in many ways. Nevertheless, how social context influences behavioural strategies and individual personality variation has rarely been addressed. This study sheds light on the relationship between social interactions, personality variation and plasticity in a collective context. For this purpose, we used a binary setup (i.e. an arena with two identical shelters) to study the aggregation process of cockroaches. We tested the same individuals in isolated and social (groups of 16 individuals) conditions. We show that even if social interactions reduce the observation of personality variation, the behaviour in a group is correlated to individual preferences displayed in isolation. Furthermore, our results suggest that individuals show different levels of plasticity according to their shelter occupancy; individuals with high occupancy rates show low levels of plasticity and are less affected by social amplification in social conditions.

The interplay between personalities and social interactions affects the cohesion of the group and the speed of aggregation.

Collective decision-making plays a central role in group-living animals and can be crucial to the survival of a group and the fitness of its members. As group-level properties emerge from individual decisions, personality variation can be a major determinant of collective behaviours. Here, we explore the relationship between personality and social interactions to explain the speed and cohesion of collective decision making during the aggregation process of the American cockroach (Periplaneta americana). We composed groups solely with shy individuals (spending a long time sheltered) or bold individuals (spending a short time sheltered) and tested them in a binary setup (arena with two shelters) for 3 consecutive days. We analysed the shelter use of individuals and groups to compare behavioural consistency among days and analyse the collective decision-making process. Contrary to the bold groups, shy groups had a faster aggregation process with more individuals sheltered mainly because shy individuals found the shelter more rapidly. Moreover, we show that personality is modulated by social interactions. We show high behavioural plasticity in bold groups, where some individuals act shy. This also suggests that learning and regulation mechanisms may take place. This study sheds some light on the implications of individual personality for collective decision making and the key role of shy individuals in gregarious species, such as P. americana.

Group choices seemingly at odds with individual preferences.

Numerous studies have focused on the influence of the social environment and the interactions between individuals on the collective decision-making of groups. They showed, for example, that attraction between individuals is at the origin of an amplification of individual preferences. These preferences may concern various environmental cues such as biomolecules that convey information about the environment such as vanillin, which, for some insects, is an attractant. In this study, we analysed how the social context of the cockroaches of the species Periplaneta americana modifies preferences when individuals are offered two shelters, of which one is vanillin scented. One of the principal results of our study is that isolated individuals stay longer and more frequently in a vanillin-scented shelter, while groups choose more frequently the unscented one. Moreover, the proportion of sheltered insects is larger when the group selects the unscented shelter. Our experimental results and theoretical model suggest that the individual preference is not inverted when insects are in a group but, rather, the response to vanillin decreases the attraction between individuals. As a result, aggregation is favoured in the unscented shelter, leading therefore to a collective inversion.

Group personality during collective decision-making: a multi-level approach.

Collective decision-making processes emerge from social feedback networks within a group. Many studies on collective behaviour underestimate the role of individual personality and, as a result, personality is rarely analysed in the context of collective dynamics. Here, we show evidence of sheltering behaviour personality in a gregarious insect (Periplaneta americana), which is characterized by a collective personality at the group level. We also highlight that the individuals within groups exhibited consistent personality traits in their probability of sheltering and total time sheltered during the three trials over one week. Moreover, the group personality, which arises from the synergy between the distribution of behaviour profiles in the group and social amplifications, affected the sheltering dynamics. However, owing to its robustness, personality did not affect the group probability of reaching a consensus. Finally, to prove social interactions, we developed a new statistical method that will be helpful for future research on personality traits and group behaviour. This approach will help to identify the circumstances under which particular group compositions may improve the fitness of individuals in gregarious species.