Social intolerance is a consequence, not a cause, of dispersal in spiders

Abstract

From invertebrates to vertebrates, a wealth of species display transient sociality during their life cycle. Investigating the causes of dispersal in temporary associations is important to better understand population dynamics. It is also essential to identify possible mechanisms involved in the evolutionary transition from transient to stable sociality, which has been documented repeatedly across taxa and typically requires the suppression of dispersal. In many animals, the onset of dispersal during ontogeny coincides with a sharp decline in social tolerance, but the causal relationship still remains poorly understood. Spiders offer relevant models to explore this question, because the adults of the vast majority of species (>48,000) are solitary and aggressive, but juveniles of most (if not all) species are gregarious and display amicable behaviors. We deployed a combination of behavioral, chemical, and modelling approaches in spiderlings of a solitary species to investigate the mechanisms controlling the developmental switch leading to the decline of social cohesion and the loss of tolerance. We show that maturation causes an increase in mobility that is sufficient to elicit dispersal without requiring any change in social behaviors. Our results further demonstrate that social isolation following dispersal triggers aggressiveness in altering the processing of conspecifics’ cues. We thus provide strong evidence that aggression is a consequence, not a cause, of dispersal in spiderlings. Overall, this study highlights the need of extended social interactions to preserve tolerance, which opens new perspectives for understanding the routes to permanent sociality.

Family-specific chemical profiles provide potential kin recognition cues in the sexually cannibalistic spider Argiope bruennichi

“…We know little about the mechanisms that underlie kin recognition in spiders, but behavioural studies indicate that it is mediated by chemical cues. This is supported by the detection of family-specific cuticular chemical profiles in spiderlings of both subsocial and solitary species [33,34]. Cuticular chemical profiles of A. bruennichi are complex in both males and females, including diverse hydrocarbons and large amounts of unusual long-chained esters, so-called wax esters (WEs) ( [35], this study).…”

“…Learning templates from other individuals is only reliable when the risk of erroneously sampling unrelated individuals is low and when phenotypes do not change over time. Family-specific cuticular profiles in spiderlings have been found in both subsocial and solitary spiders [33,34], and kin recognition occurs during the gregarious phase in some species [18][19][20][21]. However, in the subsocial Stegodyphus lineatus (Eresidae), chemical profiles of spiderlings change markedly at the onset of dispersal from the egg-sac [33], suggesting that template formation from siblings during the gregarious phase after hatching may not be practical for kin discrimination as adults.…”

Observations of dispersal in the brown recluse spider, Loxosceles reclusa (Araneae: Sicariidae)

“…Our study shows that brown recluse spiders do disperse from preferred habitat into unsuitable habitat, presumably, in a search of new areas to colonize. The preponderance of immature brown recluse spiders and the correlation of emigrants with higher populations in the garage offers some support for this conclusion (though see Chiara et al 2019). The fact that all adults captured were male is consistent with the generally higher activity and longer movements of males recorded in many species, including brown recluse spiders (Cramer & Hileman 2018).…”

Comparative transcriptomics highlights convergent evolution of energy metabolic pathways in group-living spiders

“…In theory, spiders may also form stable groups when there is an unlimited energy supply ( Figure 6 ). However, a recent study has emphasized the importance of social interaction in the route to permanent sociality, and found that reduction in the level of starvation failed to repress the aggressiveness triggered by social isolation ( Chiara et al, 2019 ). Another study denoted that underfed colonies dispersed significantly earlier than colonies fed without restriction ( Krafft et al, 1986 ).…”