Role and variability of response thresholds in the regulation of division of labor in insect societies

Author(s):  
Eric Bonabeau ◽  
Guy Theraulaz
Author(s):  
Heikki Helanterä

If the logic of natural selection is applied strictly at the level of individual production of offspring, sterile workers in insect societies are enigmatic. How can natural selection ever produce individuals that refrain from reproduction, and how are traits of such individuals that never produce offspring scrutinized and changed through natural selection? The solution to both questions is found in the family structures of insect societies. That is, the sterile helper individuals are evolutionary altruists that give up their own reproduction and instead are helping their kin reproduce and proliferate shared genes in the offspring of the fertile queen. Selection in such cases is not just a matter of individual’s direct reproduction, and instead of own offspring, the currency of the evolutionary success of sterile individuals is inclusive fitness. The concept of inclusive fitness and the process of kin selection are key to understanding the magnificent cooperation we see in insect societies, and reciprocally, insect societies are key case studies of inclusive fitness logic. In extreme cases, such as the highly advanced and sophisticated societies of ants, honeybees, and termites, the division of labor and interdependence of colony members is so complete, that it is justified to talk about a new level of evolutionary individuality. Such increases in the hierarchical complexity of life are called major transitions in evolution. We see adaptations of the colony, rather than individuals, in, e.g., their communication and group behaviors. The division of labor between morphologically differentiated queens and workers is analogous to germline-soma separation of a multicellular organism, justifying the term superorganism for the extreme cases of social lifestyle. Alongside these extreme cases, there is enormous diversity in the social lifestyles across social insect taxa, which provides a window into the balance of cooperation and conflict, and individual reproduction and helping others, in social evolution. Over the last decades, social insect research has been an area where the theoretical and empirical understanding have been developed hand in hand, together with examples of wonderful natural history, and has tremendously improved our understanding of evolution.


2017 ◽  
Author(s):  
Romain Libbrecht ◽  
Peter R. Oxley ◽  
Daniel J. C. Kronauer

AbstractDivision of labor between reproductive queens and non-reproductive workers that perform brood care is the hallmark of insect societies. However, the molecular basis of this fundamental dichotomy remains poorly understood, in part because the caste of an individual cannot typically be experimentally manipulated at the adult stage. Here we take advantage of the unique biology of the clonal raider ant, Ooceraea biroi, where reproduction and brood care behavior can be experimentally manipulated in adults. To study the molecular regulation of reproduction and brood care, we induced transitions between both states, and monitored brain gene expression at multiple time points. We found that introducing larvae that inhibit reproduction and induce brood care behavior caused much faster changes in adult gene expression than removing larvae. The delayed response to the removal of the larval signal prevents untimely activation of reproduction in O. biroi colonies. This resistance to change when removing a signal also prevents premature modifications in many other biological processes. Furthermore, we found that the general patterns of gene expression differ depending on whether ants transition from reproduction to brood care or vice versa, indicating that gene expression changes between phases are cyclic rather than pendular. Our analyses also identify genes with large and early expression changes in one or both transitions. These genes likely play upstream roles in regulating reproduction and behavior, and thus constitute strong candidates for future molecular studies of the evolution and regulation of reproductive division of labor in insect societies.


PLoS Biology ◽  
2021 ◽  
Vol 19 (6) ◽  
pp. e3001305
Author(s):  
Ingrid Fetter-Pruneda ◽  
Taylor Hart ◽  
Yuko Ulrich ◽  
Asaf Gal ◽  
Peter R. Oxley ◽  
...  

Oxytocin/vasopressin-related neuropeptides are highly conserved and play major roles in regulating social behavior across vertebrates. However, whether their insect orthologue, inotocin, regulates the behavior of social groups remains unknown. Here, we show that in the clonal raider ant Ooceraea biroi, individuals that perform tasks outside the nest have higher levels of inotocin in their brains than individuals of the same age that remain inside the nest. We also show that older ants, which spend more time outside the nest, have higher inotocin levels than younger ants. Inotocin thus correlates with the propensity to perform tasks outside the nest. Additionally, increasing inotocin pharmacologically increases the tendency of ants to leave the nest. However, this effect is contingent on age and social context. Pharmacologically treated older ants have a higher propensity to leave the nest only in the presence of larvae, whereas younger ants seem to do so only in the presence of pupae. Our results suggest that inotocin signaling plays an important role in modulating behaviors that correlate with age, such as social foraging, possibly by modulating behavioral response thresholds to specific social cues. Inotocin signaling thereby likely contributes to behavioral individuality and division of labor in ant societies.


PLoS ONE ◽  
2019 ◽  
Vol 14 (3) ◽  
pp. e0213618 ◽  
Author(s):  
Darcy Greer Gordon ◽  
Alejandra Zelaya ◽  
Ignacio Arganda-Carreras ◽  
Sara Arganda ◽  
James F. A. Traniello

2020 ◽  
Author(s):  
Qian Sun ◽  
Jordan D. Hampton ◽  
Kenneth F. Haynes ◽  
Austin Merchant ◽  
Xuguo Zhou

AbstractReproductive conflicts are common in insect societies where helping castes retain reproductive potential. One of the mechanisms regulating the conflicts is policing, a coercive behavior that reduces direct reproduction by other individuals. In eusocial Hymenoptera (ants, bees, and wasps), workers or the queen act aggressively toward fertile workers, or destroy their eggs. In many termite species (order Blattodea), upon the death of primary queen and king, workers or nymphs can differentiate into neotenic reproductives and inherit the breeding position. During this process, competition among neotenics is inevitable, but how this conflict is resolved remains unclear. Here, we report a policing behavior that regulates reproductive division of labor in the eastern subterranean termite, Reticulitermes flavipes. Our results demonstrate that the policing behavior is a cooperative effort performed sequentially by successful neotenics and workers. A neotenic reproductive initiates the attack of the fellow neotenic by biting and displays alarm behavior. Workers are then recruited to cannibalize the injured neotenic. Furthermore, the initiation of policing is age-dependent, with older reproductives attacking younger ones, thereby inheriting the reproductive position. This study provides empirical evidence of policing behavior in termites, which represents a convergent trait shared between eusocial Hymenoptera and Blattodea.


Author(s):  
Eric Bonabeau ◽  
Marco Dorigo ◽  
Guy Theraulaz

Many species of social insects have a division of labor. The resilience of task allocation exhibited at the colony level is connected to the elasticity of individual workers. The behavioral repertoire of workers can be stretched back and forth in response to perturbations. A model based on response thresholds connects individual-level plasticity with colony-level resiliency and can account for some important experimental results. Response thresholds refer to likelihood of reacting to task-associated stimuli. Low-threshold individuals perform tasks at a lower level of stimulus than high-threshold individuals. An extension of this model includes a simple form of learning. Within individual workers, performing a given task induces a decrease of the corresponding threshold, and not performing the task induces an increase of the threshold. This double reinforcement process leads to the emergence of specialized workers, that is, workers that are more responsive to stimuli associated with particular task requirements, from a group of initially identical individuals. The fixed response threshold model can be used to allocate tasks in a multiagent system, in a way that is similar to market-based models, where agents bid to get resources or perform tasks. The response threshold model with learning can be used to generate differentiation in task performance in a multiagent system composed of initially identical entities. Task allocation in this case is emergent and more robust with respect to perturbations of the system than when response thresholds are fixed. An example application to distributed mail retrieval is presented. In social insects, different activities are often performed simultaneously by specialized individuals. This phenomenon is called division of labor [253, 272]. Simultaneous task performance by specialized workers is believed to be more efficient than sequential task performance by unspecialized workers [188, 253]. Parallelism avoids task switching, which costs energy and time. Specialization allows greater efficiency of individuals in task performance because they “know” the task or are better equipped for it. All social insects exhibit reproductive division of labor: only a small fraction of the colony, often limited to a single individual, reproduces.


Author(s):  
Samuel N. Beshers ◽  
Gene E. Robinson ◽  
Jay E. Mittenthal

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