Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus

Colony size is a fundamental attribute of insect societies that appears to play an important role in their organization of work. In the harvester ant Pogonomyrmex californicus, division of labor increases with colony size during colony ontogeny and among unmanipulated colonies of the same age. However, the mechanism(s) integrating individual task specialization and colony size is unknown. To test whether the scaling of division of labor is an emergent epiphenomenon, as predicted by self-organizational models of task performance, we manipulated colony size in P. californicus and quantified short-term behavioral responses of individuals and colonies. Variation in colony size failed to elicit a change in division of labor, suggesting that colony-size effects on task specialization are mediated by slower developmental processes and/or correlates of colony size that were missing from our experiment. In contrast, the proportional allocation of workers to tasks shifted with colony size, suggesting that task needs or priorities depend, in part, on colony size alone. Finally, although task allocation was flexible, colony members differed consistently in task performance and spatial tendency across colony size treatments. Sources of interindividual behavioral variability include worker age and genotype (matriline).     

Implications of behavioral architecture for the evolution of self-organized division of labor

Division of labor has been studied separately from a proximate self-organization and an ultimate evolutionary perspective. We aim to bring together these two perspectives. So far this has been done by choosing a behavioral mechanism a priori and considering the evolution of the properties of this mechanism. Here we use artificial neural networks to allow for a more open architecture. We study whether emergent division of labor can evolve in two different network architectures; a simple feedforward network, and a more complex network that includes the possibility of self-feedback from previous experiences. We focus on two aspects of division of labor; worker specialization and the ratio of work performed for each task. Colony fitness is maximized by both reducing idleness and achieving a predefined optimal work ratio. Our results indicate that architectural constraints play an important role for the outcome of evolution. With the simplest network, only genetically determined specialization is possible. This imposes several limitations on worker specialization. Moreover, in order to minimize idleness, networks evolve a biased work ratio, even when an unbiased work ratio would be optimal. By adding self-feedback to the network we increase the network's flexibility and worker specialization evolves under a wider parameter range. Optimal work ratios are more easily achieved with the self-feedback network, but still provide a challenge when combined with worker specialization.     

The Evolution of Different Forms of Sociality: Behavioral Mechanisms and Eco-Evolutionary Feedback

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from “leader-follower” societies to “fission-fusion” societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.     

The making of a social insect: developmental architectures of social design

We marvel at the social complexity of insects, marked by anatomically and behaviorally distinguishable castes, division of labor and specialization—but how do such systems evolve? Insect societies are composed of individuals, each undergoing its own developmental process and each containing its own genetic information and experiencing its own developmental and experiential environment. Yet societies appear to function as if the colonies themselves are individuals with novel “social genes” and novel social developmental processes. We propose an alternative hypothesis. The origins of complex social behavior, from which insect societies emerge, are derived from ancestral developmental programs. These programs originated in ancient solitary insects and required little evolutionary remodeling. We present evidence from behavioral assays, selective breeding, genetic mapping, functional genomics and endocrinology, and comparative anatomy and physiology. These insights explain how complex social behavior can evolve from heterochronic changes in reproductive signaling systems that govern ubiquitous and ancient relationships between behavior and ovarian development. BioEssays 29:334–343, 2007. © 2007 Wiley Periodicals, Inc.     

Geometry Shapes Evolution of Early Multicellularity

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units in which reproduction is the sole responsibility of a subset of units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular “snowflake-like” cluster formed in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.     

Specialization Does Not Predict Individual Efficiency in an Ant

The ecological success of social insects is often attributed to an increase in efficiency achieved through division of labor between workers in a colony. Much research has therefore focused on the mechanism by which a division of labor is implemented, i.e., on how tasks are allocated to workers. However, the important assumption that specialists are indeed more efficient at their work than generalist individuals—the “Jack-of-all-trades is master of none” hypothesis—has rarely been tested. Here, I quantify worker efficiency, measured as work completed per time, in four different tasks in the ant Temnothorax albipennis: honey and protein foraging, collection of nest-building material, and brood transports in a colony emigration. I show that individual efficiency is not predicted by how specialized workers were on the respective task. Worker efficiency is also not consistently predicted by that worker''s overall activity or delay to begin the task. Even when only the worker''s rank relative to nestmates in the same colony was used, specialization did not predict efficiency in three out of the four tasks, and more specialized workers actually performed worse than others in the fourth task (collection of sand grains). I also show that the above relationships, as well as median individual efficiency, do not change with colony size. My results demonstrate that in an ant species without morphologically differentiated worker castes, workers may nevertheless differ in their ability to perform different tasks. Surprisingly, this variation is not utilized by the colony—worker allocation to tasks is unrelated to their ability to perform them. What, then, are the adaptive benefits of behavioral specialization, and why do workers choose tasks without regard for whether they can perform them well? We are still far from an understanding of the adaptive benefits of division of labor in social insects.     

Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae)

The evolution of complex societies with obligate reproductive division of labor represents one of the major transitions in evolution. In such societies, functionally sterile individuals (workers) perform many of fitness‐relevant behaviors including allomaternal ones, without getting any direct fitness benefits. The question of how such worker division of labor has evolved remains controversial. The reproductive groundplan hypothesis (RGPH) offers a powerful proximate explanation for this evolutionary leap. The RGPH argues that the conserved genetic and endocrinological networks regulating fitness‐relevant behavior (e g. foraging and brood care) in their solitary ancestors have become decoupled from actual reproduction in the worker caste and now generate worker behavioral phenotypes. However, the empirical support for this hypothesis remains limited to a handful of species making its general validity uncertain. In this study, we combine data from the literature with targeted sampling of key species and apply phylogenetically controlled comparative analysis to investigate if the key prediction of the RGPH, namely an association between allomaternal behavior and an allomaternal physiological state holds in the largest and most species‐rich clade of social insects, the ants. Our findings clearly support the RPGH as a general framework to understand the evolution of the worker caste and shed light on one of the major transition in evolutionary history.     

Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies

Within-group communication is a fundamental feature of animal societies. In order for animal groups to function as adaptive units, the members must share information such that group mates respond appropriately to each others’ behavior. One important function of social communication is to affect the allocation of tasks among group members. Theoretical and empirical findings on a diverse array of social insect taxa show that interactions among workers often play important roles in structuring division of labor. We review worker interactions that regulate division of labor in insect societies, which we refer to as worker connectivity. We present a framework for synthesizing and analyzing the study of worker connectivity. The widespread reliance on worker connectivity among eusocial insect taxa and the diversity of communicative mechanisms used to recruit workers suggest that the nature of worker interactions has evolved by natural selection. We suggest that colony-level selection acting on variation in task allocation has been an important force in the evolution of mechanisms for worker connectivity. We also propose that there are important links between individual worker cognition and task allocation at the colony level. Evolutionary changes in the cognitive aspects of worker responses may affect task allocation as much as changes in the communicative signals themselves. Received 9 December 2006; revised 18 May 2007; accepted 30 May 2007.     

Emergence and Consequences of Division of Labor in Associations of Normally Solitary Sweat Bees

Division of labor is a pervasive feature of animal societies, but little is known about the causes or consequences of division of labor in non-eusocial cooperative groups. We tested whether division of labor self-organizes in an incipient social system: artificially induced nesting associations of the normally solitary sweat bee Lasioglossum ( Ctenonomia ) NDA-1 (Hymenoptera: Halictidae). We quantified task performance and construction output by females nesting either alone or with a conspecific. Within pairs, a division of labor repeatedly arose in which one individual specialized on excavation and pushing/tamping while her nestmate guarded the nest entrance. Task specialization could not be attributed to variation in overall activity, and the degree of behavioral differentiation was greater than would be expected due to random variation, indicating that division of labor was an emergent phenomenon generated in part by social dynamics. Excavation specialists did not incur a survival cost, in contrast to previous findings for ant foundress associations. Paired individuals performed more per capita guarding, and pairs collectively excavated deeper nests than single bees – potential early advantages of social nesting in halictine bees.     

Teams in animal societies

We review the existence of teams in animal societies. Teamshave previously been dismissed in all but a tiny minority ofinsect societies. "Team" is a term not generally used in studiesof vertebrates. We propose a new rigorous definition of a teamthat may be applied to both vertebrate and invertebrate societies.We reconsider what it means to work as a team or group andsuggest that there are many more teams in insect societies than previously thought. A team task requires different subtasksto be performed concurrently for successful completion. Thereis a division of labor within a team. Contrary to previousreviews of teams in social insects, we do not constrain teamsto consist of members of different castes and argue that teammembers may be interchangeable. Consequently, we suggest thata team is simply the set of individuals that performs a teamtask. We contrast teams with groups and suggest that a grouptask requires the simultaneous performance and cooperationof two or more individuals for successful completion. In agroup, there is no division of labor—each individual performs the same task. We also contrast vertebrate and invertebrateteams and find that vertebrate teams tend to be associatedwith hunting and are based on individual recognition. Invertebrateteams occur in societies characterized by a great deal of redundancy,and we predict that teams in insect societies are more likelyto be found in large polymorphic ("complex") societies thanin small monomorphic ("simple") societies.     

Fine Individual Specialization and Elitism among Workers of the Ant Ectatomma tuberculatum for a Highly Specific Task: Intruder Removal

Insect societies are characterized by a relatively sophisticated division of labor; they form tightly knit groups that must effectively exclude non‐members from the colony. However, the Neotropical predatory ant Ectatomma tuberculatum can harbor several specific myrmecophiles and, in particular, various eucharitid parasitoid wasp species. Adult wasps eclose in the host nests and are removed by worker ants without harm. Previous observations suggest that only a few workers perform this task. To test this hypothesis, we introduced different types of intruders, live and dead, pentane‐washed broad‐nosed grain weevil individuals (Caulophilus oryzae) and dead, pentane‐washed eucharitids (Dilocantha lachaudii), into laboratory colonies containing individually marked workers. We recorded all encounters and behaviors until the intruders were removed. Certain workers removed intruders more frequently than expected by chance. The number of encounters with an intruder was positively correlated with the number of removals performed by the workers. For each nest, a small group of workers was identified as specialized in intruder removal. A subset of very committed workers in the specialists group that performed up to 57% of removals qualified as hyperspecialists or elite workers. The behavioral sequences differed based on the type and condition of the intruder: the sequence was more complex and included numerous aggressive behaviors (mandibular strikes and attempts at stinging) when workers encountered a live weevil. In contrast, the behavioral sequences with dead, pentane‐washed insects were characterized by numerous detections through contact that did not lead to rejection and by the intruders simply being seized and removed from the nest. Overall, the data show that the ants discriminated between live and pentane‐washed intruders and adjusted their behavior accordingly. This is the first demonstration in ants of both behavioral specialization and hyperspecialization in intruder removal.     

Individual experience alone can generate lasting division of labor in ants

Division of labor, the specialization of workers on different tasks, largely contributes to the ecological success of social insects [1, 2]. Morphological, genotypic, and age variations among workers, as well as their social interactions, all shape division of labor [1-12]. In addition, individual experience has been suggested to influence workers in their decision to execute a task [13-18], but its potential impact on the organization of insect societies has yet to be demonstrated [19, 20]. Here we show that, all else being equal, ant workers engaged in distinct functions in accordance with their previous experience. When individuals were experimentally led to discover prey at each of their foraging attempts, they showed a high propensity for food exploration. Conversely, foraging activity progressively decreased for individuals who always failed in the same situation. One month later, workers that previously found prey kept on exploring for food, whereas those who always failed specialized in brood care. It thus appears that individual experience can strongly channel the behavioral ontogeny of ants to generate a lasting division of labor. This self-organized task-attribution system, based on an individual learning process, is particularly robust and might play an important role in colony efficiency.     

Worker brain development and colony organization in ants: Does division of labor influence neuroplasticity?

Brain compartment size allometries may adaptively reflect cognitive needs associated with behavioral development and ecology. Ants provide an informative system to study the relationship of neural architecture and development because worker tasks and sensory inputs may change with age. Additionally, tasks may be divided among morphologically and behaviorally differentiated worker groups (subcastes), reducing repertoire size through specialization and aligning brain structure with task‐specific cognitive requirements. We hypothesized that division of labor may decrease developmental neuroplasticity in workers due to the apparently limited behavioral flexibility associated with task specialization. To test this hypothesis, we compared macroscopic and cellular neuroanatomy in two ant sister clades with striking contrasts in worker morphological differentiation and colony‐level social organization: Oecophylla smaragdina , a socially complex species with large colonies and behaviorally distinct dimorphic workers, and Formica subsericea , a socially basic species with small colonies containing monomorphic workers. We quantified volumes of functionally distinct brain compartments in newly eclosed and mature workers and measured the effects of visual experience on synaptic complex (microglomeruli) organization in the mushroom bodies—regions of higher‐order sensory integration—to determine the extent of experience‐dependent neuroplasticity. We demonstrate that, contrary to our hypothesis, O. smaragdina workers have significant age‐related volume increases and synaptic reorganization in the mushroom bodies, whereas F. subsericea workers have reduced age‐related neuroplasticity. We also found no visual experience‐dependent synaptic reorganization in either species. Our findings thus suggest that changes in the mushroom body with age are associated with division of labor, and therefore social complexity, in ants. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1072–1085, 2017     

Division of Labor Regulates Precision Rescue Behavior in Sand-Dwelling Cataglyphis cursor Ants: To Give Is to Receive

Division of labor, an adaptation in which individuals specialize in performing tasks necessary to the colony, such as nest defense and foraging, is believed key to eusocial insects'' remarkable ecological success. Here we report, for the first time, a completely novel specialization in a eusocial insect, namely the ability of Cataglyphis cursor ants to rescue a trapped nestmate using precisely targeted behavior. Labeled “precision rescue”, this behavior involves the ability of rescuers not only to detect what, exactly, holds the victim in place, but also to direct specific actions to this obstacle. Individual ants, sampled from each of C. cursor''s three castes, namely foragers, nurses and inactives, were experimentally ensnared (the “victim”) and exposed to a caste-specific group of potential “rescuers.” The data reveal that foragers were able to administer, and obtain, the most help while members of the youngest, inactive caste not only failed to respond to victims, but also received virtually no help from potential rescuers, regardless of caste. Nurses performed intermediate levels of aid, mirroring their intermediate caste status. Our results demonstrate that division of labor, which controls foraging, defense and brood care in C. cursor, also regulates a newly discovered behavior in this species, namely a sophisticated form of rescue, a highly adaptive specialization that is finely tuned to a caste member''s probability of becoming, or encountering, a victim in need of rescue.     

Reappraising Social Insect Behavior through Aversive Responsiveness and Learning

Background

The success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower thresholds specialize in this task. This model is at odds with findings on honeybee behavior as nectar and pollen foragers exhibit different responsiveness to sucrose, with nectar foragers having higher response thresholds to sucrose concentration. Moreover, it has been suggested that sucrose responsiveness correlates with responsiveness to most if not all other stimuli. If this is the case, explaining task specialization and the origins of division of labor on the basis of differences in response thresholds is difficult.

Methodology

To compare responsiveness to stimuli presenting clear-cut differences in hedonic value and behavioral contexts, we measured appetitive and aversive responsiveness in the same bees in the laboratory. We quantified proboscis extension responses to increasing sucrose concentrations and sting extension responses to electric shocks of increasing voltage. We analyzed the relationship between aversive responsiveness and aversive olfactory conditioning of the sting extension reflex, and determined how this relationship relates to division of labor.

Principal Findings

Sucrose and shock responsiveness measured in the same bees did not correlate, thus suggesting that they correspond to independent behavioral syndromes, a foraging and a defensive one. Bees which were more responsive to shock learned and memorized better aversive associations. Finally, guards were less responsive than nectar foragers to electric shocks, exhibiting higher tolerance to low voltage shocks. Consequently, foragers, which are more sensitive, were the ones learning and memorizing better in aversive conditioning.

Conclusions

Our results constitute the first integrative study on how aversive responsiveness affects learning, memory and social organization in honeybees. We suggest that parallel behavioral modules (e.g. appetitive, aversive) coexist within each individual bee and determine its tendency to adopt a given task. This conclusion, which is at odds with a simple threshold model, should open new opportunities for exploring the division of labor in social insects.     

Is There Division of Labor in Cooperative Pseudoscorpions? An Analysis of the Behavioral Repertoire of a Tropical Species

Division of labor is a strategy that maximizes the foraging and reproductive success of eusocial insects. Although some arachnids exhibit colony structure and social organization similar to that of hymenopterans, temporal polyethism has only been demonstrated in few species. The social organization of cooperative pseudoscorpions Paratemnoides nidificator is similar to that of social spiders, but it involves a clear division of labor. Work allocation was experimentally investigated in colonies composed of only one developmental stage (young or adults) or by one sex (males or females), through laboratory manipulation. During 44 h of observation, more than 14 000 behavioral repetitions were quantified, distributed in 95 different types of behavioral acts, and grouped in 10 behavioral categories. The results showed that reproductive colonies of P. nidificator are maintained by gender‐ and age‐based activities. Males and non‐reproductive females performed the external cleaning of the colony and prey capture. Reproductive females take care of the juveniles and build reproductive silk chambers. Nymphs build most of the molt chambers and perform internal cleaning. In the absence of nymphs, male colonies survived 1–2 mo, while female colonies survived 3–4 mo. In nymph colonies, work is readjusted so that all maintenance tasks are executed. This is the first study clearly demonstrating division of tasks in arachnids. It suggests that specialization is an adaptative and evolutionarily old trait in this species. Unlike cooperative spiders, P. nidificator possesses physiological (e.g. reproduction, ecdysis, lifespan) and behavioral (e.g. behavioral synchrony or self‐organization) characteristics that allow task specialization.     

The Evolutionary Origin of Somatic Cells under the Dirty Work Hypothesis

Reproductive division of labor is a hallmark of multicellular organisms. However, the evolutionary pressures that give rise to delineated germ and somatic cells remain unclear. Here we propose a hypothesis that the mutagenic consequences associated with performing metabolic work favor such differentiation. We present evidence in support of this hypothesis gathered using a computational form of experimental evolution. Our digital organisms begin each experiment as undifferentiated multicellular individuals, and can evolve computational functions that improve their rate of reproduction. When such functions are associated with moderate mutagenic effects, we observe the evolution of reproductive division of labor within our multicellular organisms. Specifically, a fraction of the cells remove themselves from consideration as propagules for multicellular offspring, while simultaneously performing a disproportionately large amount of mutagenic work, and are thus classified as soma. As a consequence, other cells are able to take on the role of germ, remaining quiescent and thus protecting their genetic information. We analyze the lineages of multicellular organisms that successfully differentiate and discover that they display unforeseen evolutionary trajectories: cells first exhibit developmental patterns that concentrate metabolic work into a subset of germ cells (which we call “pseudo-somatic cells”) and later evolve to eliminate the reproductive potential of these cells and thus convert them to actual soma. We also demonstrate that the evolution of somatic cells enables phenotypic strategies that are otherwise not easily accessible to undifferentiated organisms, though expression of these new phenotypic traits typically includes negative side effects such as aging.     

Incomplete division of labor: error-prone multitaskers coexist with specialists

Division of labor (DoL) occurs when individual members of a group specialize by performing particular tasks toward some common goal. Under complete DoL, every individual acts as a specialist and so performs only one kind of task. But under incomplete DoL, some individuals may act as generalists and so have the capacity to perform more than one kind of task. This persistence of generalists in the presence of specialists presents a theoretical challenge, particularly if generalists must pay an extra cost, an inefficiency penalty, for their capacity to perform more than one type of task. Prior work focused on how such costs tend to drive evolution toward complete DoL, with only specialists typically remaining at equilibrium [Wahl, L.M., 2002a. Evolving the division of labor: generalists, specialists and task allocation. J. Theoret. Biol. 219, 371-388; Wahl, L.M., 2002b. The division of labor: genotypic versus phenotypic specialization. Am. Nat. 160, 135-145]. Relaxing this key assumption, we show that generalists, despite paying some extra costs, can coexist with specialists. Relaxing another assumption, we also show that this coexistence can hold even when generalists often perform the wrong task. How can stable multitasking emerge despite this flawed decision-making? From the perspective that cognitive errors matter only when they translate into fitness decrements, we observe that error-prone generalists may persist most commonly in situations in which their mistakes do little to jeopardize group success. Our findings show that incomplete DoL can emerge even when generalists often err and must pay extra costs for their multitasking capacity.     

Rapid Transition towards the Division of Labor via Evolution of Developmental Plasticity

A crucial step in several major evolutionary transitions is the division of labor between components of the emerging higher-level evolutionary unit. Examples include the separation of germ and soma in simple multicellular organisms, appearance of multiple cell types and organs in more complex organisms, and emergence of casts in eusocial insects. How the division of labor was achieved in the face of selfishness of lower-level units is controversial. I present a simple mathematical model describing the evolutionary emergence of the division of labor via developmental plasticity starting with a colony of undifferentiated cells and ending with completely differentiated multicellular organisms. I explore how the plausibility and the dynamics of the division of labor depend on its fitness advantage, mutation rate, costs of developmental plasticity, and the colony size. The model shows that the transition to differentiated multicellularity, which has happened many times in the history of life, can be achieved relatively easily. My approach is expandable in a number of directions including the emergence of multiple cell types, complex organs, or casts of eusocial insects.