Response thresholds alone cannot explain empirical patterns of division of labor in social insects

Abstract

The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.

An oxytocin/vasopressin-related neuropeptide modulates social foraging behavior in the clonal raider ant

“…This cycle is regulated by the presence of larvae, which suppress reproduction and induce brood care behavior (i.e., foraging and nursing) in the adults [46,[48][49][50]. Moreover, as in other social insects, the propensity to forage correlates with age, with older ants performing more tasks outside the nest than younger ants (age polyethism) [51]. Finally, workers have a variable number of ovarioles, which correlates with behavior, with regular workers (2 or 3 ovarioles) performing more foraging activity than intercastes (4 or more ovarioles) [51].…”

“…Finally, workers have a variable number of ovarioles, which correlates with behavior, with regular workers (2 or 3 ovarioles) performing more foraging activity than intercastes (4 or more ovarioles) [51]. Moreover, in O. biroi, stable division of labor emerges even among workers that are matched for genotype, age, and reproductive physiology, suggesting underlying variation in behavioral response thresholds [20,51].…”

“…Moreover, as in other social insects, the propensity to forage correlates with age, with older ants performing more tasks outside the nest than younger ants (age polyethism) [ 51 ]. Finally, workers have a variable number of ovarioles, which correlates with behavior, with regular workers (2 or 3 ovarioles) performing more foraging activity than intercastes (4 or more ovarioles) [ 51 ]. Moreover, in O .…”

“…Moreover, in O . biroi , stable division of labor emerges even among workers that are matched for genotype, age, and reproductive physiology, suggesting underlying variation in behavioral response thresholds [ 20 , 51 ].…”

Environment dependent benefits of inter-individual variation in honey bee recruitment

“…Unfortunately, the focus on response thresholds has come at the cost of neglecting other response parameters that may be important for division of labour, like response probability and intensity (Cook et al, 2020;Jeanson and Weidenmüller, 2013;Ulrich et al, 2021). An individual's task performance for a given stimulus intensity is a combination of both its probability of responding to the stimulus and the intensity of its response, either in terms of the number or duration of response events Weidenmüller, 2004).…”