Individual versus social complexity, with particular reference to ant colonies

Insect societies colonies of ants, bees, wasps and termites--vary enormously in their social complexity. Social complexity is a broadly used term that encompasses many individual and colony-level traits and characteristics such as colony size, polymorphism and foraging strategy. A number of earlier studies have considered the relationships among various correlates of social complexity in insect societies; in this review, we build upon those studies by proposing additional correlates and show how all correlates can be integrated in a common explanatory framework. The various correlates are divided among four broad categories (sections). Under 'polyphenism' we consider the differences among individuals, in particular focusing upon 'caste' and specialization of individuals. This is followed by a section on 'totipotency' in which we consider the autonomy and subjugation of individuals. Under this heading we consider various aspects such as intracolony conflict, worker reproductive potential and physiological or morphological restrictions which limit individuals' capacities to perform a range of tasks or functions. A section entitled 'organization of work' considers a variety of aspects, e.g. the ability to tackle group, team or partitioned tasks, foraging strategies and colony reliability and efficiency. A final section, 'communication and functional integration', considers how individual activity is coordinated to produce an integrated and adaptive colony. Within each section we use illustrative examples drawn from the social insect literature (mostly from ants, for which there is the best data) to illustrate concepts or trends and make a number of predictions concerning how a particular trait is expected to correlate with other aspects of social complexity. Within each section we also expand the scope of the arguments to consider these relationships in a much broader sense of'sociality' by drawing parallels with other 'social' entities such as multicellular individuals, which can be understood as 'societies' of cells. The aim is to draw out any parallels and common causal relationships among the correlates. Two themes run through the study. The first is the role of colony size as an important factor affecting social complexity. The second is the complexity of individual workers in relation to the complexity of the colony. Consequently, this is an ideal opportunity to test a previously proposed hypothesis that 'individuals of highly social ant species are less complex than individuals from simple ant species' in light of numerous social correlates. Our findings support this hypothesis. In summary, we conclude that, in general, complex societies are characterized by large colony size, worker polymorphism, strong behavioural specialization and loss of totipotency in its workers, low individual complexity, decentralized colony control and high system redundancy, low individual competence, a high degree of worker cooperation wher tackling tasks, group foraging strategies, high tempo, multi-chambered tailor-made nests, high functional integration, relatively greater use of cues and modulatory signals to coordinate individuals and heterogeneous patterns of worker-worker interaction.     

Colony size,social complexity and reproductive conflict in social insects

The broad limits of mature colony size in social insect species are likely to be set by ecological factors. However, any change in colony size has a number of important social consequences. The most fundamental is a change in the expected reproductive potential of workers. If colony size rises, workers experience a fall in their chances of becoming replacement reproductives and, it is shown, increasing selection for mutual inhibition of one another's reproduction (worker policing). As workers’ reproductive potential falls, the degree of dimorphism between reproductive and worker castes (morphological skew) can rise. This helps explain why small societies have low morphological skew and tend to be simple in organization, whereas large societies have high morphological skew and tend to be complex. The social consequences of change in colony size may also alter colony size itself in a process of positive feedback. For these reasons, small societies should be characterized by intense, direct conflict over reproduction and caste determination. By contrast, conflict in large societies should predominantly be over brood composition, and members of these societies should be relatively compliant to manipulation of their caste. Colony size therefore deserves fuller recognition as a key determinant, along with kin structure, of social complexity, the reproductive potential of helpers, the degree of caste differentiation, and the nature of within-group conflict.     

The energetic cost of reproductive conflicts in the ant Pachycondyla obscuricornis

In a variety of social animals, individuals can secure reproductive rights through aggressive dominance. Direct individual benefits of aggression are widely recognized, but underlying costs affecting group productivity, and thus indirect benefits, are less clear. Costs of aggressive regulation of reproduction are especially important in small social insect colonies, where individual workers could potentially dominate male production. We estimated the energetic costs associated with the regulation of worker reproduction in the ponerine ant Pachycondyla obscuricornis, using the total CO2 emission of a colony as a measure. The level of CO2 emission of 12 experimental colonies varied significantly during five periods with varying levels of aggression and egg-laying. Overall, CO2 emission increased with the degree of fighting in a colony, but was not associated with differences in egg-laying. Aggressive regulation of reproduction and the formation of a dominance hierarchy thus pose an energetic cost to the colony. Furthermore, workers reduce their work-activities immediately after experimental orphaning, giving a further cost to the colony. These costs might influence the outcome of conflicts over male production in ants. This paper presents the first quantification of energetic costs of aggressive behavior regulating reproduction in ants.     

Nestmate recognition and identification of cuticular hydrocarbons composition in the swarm founding paper wasp Ropalidia opifex

Eusocial polistine wasps comprise species in which new colonies are founded by single wasps or groups of foundresses (independent founding species) or by swarms of queens and workers (swarm founding species). The first ones have relatively small societies generally comprising only one egg-laying queen, while the second ones have larger colonies where several egg-laying queens are usually present. These differences in social organisation are expected to influence the acceptance threshold of conspecifics in the colony and the intra-colony communication modalities. In this paper, we showed by field experiments that Ropalidia opifex (a swarm founding species) presents a good discrimination between alien and nestmate conspecifics. Moreover by GC/MS, we identified 19 cuticular hydrocarbons in this species, and we demonstrated that cuticular signature in this species depends mainly on colony membership, not showing any correlation with fertility.     

Cuticular hydrocarbons correlated with reproductive status in a queenless ant

Reproductive division of labour is regulated behaviourally in social insects lacking morphologically specialized castes. The directional nature of dominance interactions shows that recognition occurs, but little is known about its basis. In the queenless ant Dinoponera quadriceps, the top worker in the hierarchy (''alpha'') mates and produces offspring in each colony, while other workers remain virgin. Dominant ants frequently rub one antenna of subordinates against their own cuticle, and alpha and infertile nest-mates consistently differ in their relative proportions of the cuticular hydrocarbon 9-hentriacontene (9-C₃₁). The second-ranking ''beta'' occasionally lays unfertilized eggs and we show that she has less 9-C₃₁ than the alpha but more than infertile workers. To investigate further the link between 9-C₃₁ and ovarian activity, we experimentally removed alpha workers (n=11 individuals) and used solid-phase microextraction (SPME) with gas chromatography to measure changes in 9-C₃₁ on live beta workers which attained alpha status. The proportion of 9-C₃₁ on the replacement alpha increased significantly after six weeks, in parallel with her gain in fecundity. We discuss whether 9-C₃₁ provides honest information about egg-laying ability, enabling ants to recognize the different classes of nest-mates involved in reproductive conflicts. Such fertility cues could reliably underpin the antagonistic interactions occurring in insect societies.     

Analogies in the evolution of individual and social immunity

We compare anti-parasite defences at the level of multicellular organisms and insect societies, and find that selection by parasites at these two organisational levels is often very similar and has created a number of parallel evolutionary solutions in the host's immune response. The defence mechanisms of both individuals and insect colonies start with border defences to prevent parasite intake and are followed by soma defences that prevent the establishment and spread of the parasite between the body's cells or the social insect workers. Lastly, germ line defences are employed to inhibit infection of the reproductive tissue of organisms or the reproductive individuals in colonies. We further find sophisticated self/non-self-recognition systems operating at both levels, which appear to be vital in maintaining the integrity of the body or colony as a reproductive entity. We then expand on the regulation of immune responses and end with a contemplation of how evolution may shape the different immune components, both within and between levels. The aim of this review is to highlight common evolutionary principles acting in disease defence at the level of both individual organisms and societies, thereby linking the fields of physiological and ecological immunology.     

Emergent polyethism as a consequence of increased colony size in insect societies

A threshold reinforcement model in insect societies is explored over a range of colony sizes and levels of task demand to examine their effects upon worker polyethism. We find that increasing colony size while keeping the demand proportional to the colony size causes an increase in the differentiation among individuals in their activity levels, thus explaining the occurrence of elitism (individuals that do a disproportionately large proportion of work) in insect societies. Similar results were obtained when the overall work demand is increased while keeping the colony size constant. Our model can reproduce a whole suite of distributions of the activity levels among colony members that have been found in empirical studies. When there are two tasks, we demonstrate that increasing demand and colony size generates highly specialized individuals, but without invoking any strict assumptions about spatial organization of work or any inherent abilities of individuals to tackle different tasks. Importantly, such specialization only occurs above a critical colony size such that smaller colonies contain a set of undifferentiated equally inactive individuals while larger colonies contain both active specialists and inactive generalists, as has been found in empirical studies and is predicted from other theoretical considerations.     

Worker policing limits the number of reproductives in a ponerine ant

Reproductive division of labour is an essential feature of insect sociality, but the regulation of sterility among colony members remains incompletely understood. Ant workers and queens are morphologically divergent and workers are only capable of producing males in a colony, although they usually do not do so. Worker policing is one mechanism proposed for their infertility and it can be expressed as either aggressive inhibition of ovarian activity among workers or destruction of worker-laid eggs. A few studies have shown that workers with developed ovaries are preferentially attacked by nest-mates, but adequate demonstration of worker policing also requires evidence that these attacks result in the suppression of ovarian activity or death. We investigated worker policing in the ponerine ant Harpegnathos saltator in which workers are able to mate and replace the founding queen. Five colonies were each divided into two groups, one of which consisted exclusively of infertile workers. Some individuals in the orphaned groups began laying eggs during the three-week separation and upon reunification these were vigorously attacked by infertile workers of the other groups. The ovarian activity of these new egg layers became inhibited, as revealed by subsequent dissection of marked individuals. Worker policing in H. saltator appears to function primarily in preventing an excess of reproductive workers.     

Lack of conflict during queen production in the social wasp Vespula maculifrons

Social insects display extreme cooperative and helping behaviours. However, social insect colonies are also arenas of intense competitive interactions. One particularly important matter over which colony members may compete centres on the development of sexual offspring. Specifically, colony members may engage in selfish behaviours leading to reproductive competition, whereby individuals either strive to develop as sexuals or assist kin so that close relatives emerge as new reproductives. We investigated whether reproductive competition occurred in the polyandrous social wasp Vespula maculifrons. We genotyped V. maculifrons workers and new queens at eight polymorphic microsatellite loci to determine if larvae of particular genotypes were reared as gynes more frequently than expected by chance. However, we found no significant evidence of reproductive competition in this species. The proportional contributions of males to workers and new queens did not vary within colonies. Moreover, male reproductive skew did not differ between workers and new queens. Finally, novel statistical techniques uncovered no evidence of patriline reversal, the phenomenon whereby males that contribute little to worker production contribute substantially to new queen production. Consequently, we conclude that individual level selection operating to increase the frequency of selfish behaviours that would lead to reproductive competition has been nullified by colony-level selection acting to maintain colony efficiency and cooperation.     

Social life: the paradox of multiple-queen colonies

The evolution of animal societies in which some individuals forego their own reproductive opportunities to help others to reproduce poses an evolutionary paradox that can be traced to Darwin. Altruism may evolve through kin selection when the donor and recipient of altruistic acts are related to each other, as generally is the case in social birds and mammals. Similarly, social insect workers are highly related to the brood they rear when colonies are headed by a single queen. However, recent studies have shown that insect colonies frequently contain several queens, with the effect of decreasing relatedness among colony members. How can one account for the origin and maintenance of such colonies? This evolutionary enigma presents many of the same theoretical challenges as does the evolution of cooperative breeding and eusociality.     

To b or not to b: a pheromone-binding protein regulates colony social organization in fire ants

A major distinction in the social organization of ant societies is the number of reproductive queens that reside in a single colony. The fire ant Solenopsis invicta exists in two distinct social forms, one with colonies headed by a single reproductive queen and the other containing several to hundreds of egg-laying queens. This variation in social organization has been shown to be associated with genotypes at the gene Gp-9. Specifically, single-queen colonies have only the B allelic variant of this gene, whereas multiple-queen colonies always have the b variant as well. Subsequent studies revealed that Gp-9 shares the highest sequence similarity with genes encoding pheromone-binding proteins (PBPs). In other insects, PBPs serve as central molecular components in the process of chemical recognition of conspecifics. Fire ant workers regulate the number of egg-laying queens in a colony by accepting queens that produce appropriate chemical signals and destroying those that do not. The likely role of GP-9 in chemoreception suggests that the essential distinction in colony queen number between the single and multiple-queen form originates from differences in workers' abilities to recognize queens. Other, closely related fire ant species seem to regulate colony social organization in a similar fashion.     

Subfamily‐dependent alternative reproductive strategies in worker honeybees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.     

Social Context and Reproductive Potential Affect Worker Reproductive Decisions in a Eusocial Insect

Context-dependent decision-making conditions individual plasticity and is an integrant part of alternative reproductive strategies. In eusocial Hymenoptera (ants, bees and wasps), the discovery of worker reproductive parasitism recently challenged the view of workers as a homogeneous collective entity and stressed the need to consider them as autonomous units capable of elaborate choices which influence their fitness returns. The reproductive decisions of individual workers thus need to be investigated and taken into account to understand the regulation of reproduction in insect societies. However, we know virtually nothing about the proximate mechanisms at the basis of worker reproductive decisions. Here, we test the hypothesis that the capacity of workers to reproduce in foreign colonies lies in their ability to react differently according to the colonial context and whether this reaction is influenced by a particular internal state. Using the bumble bee Bombus terrestris, we show that workers exhibit an extremely high reproductive plasticity which is conditioned by the social context they experience. Fertile workers reintroduced into their mother colony reverted to sterility, as expected. On the contrary, a high level of ovary activity persisted in fertile workers introduced into a foreign nest, and this despite more frequent direct contacts with the queen and the brood than control workers. Foreign workers'' reproductive decisions were not affected by the resident queen, their level of fertility being similar whether or not the queen was removed from the host colony. Workers'' physiological state at the time of introduction is also of crucial importance, since infertile workers failed to develop a reproductive phenotype in a foreign nest. Therefore, both internal and environmental factors appear to condition individual reproductive strategies in this species, suggesting that more complex decision-making mechanisms are involved in the regulation of worker reproduction than previously thought.     

Differentiated Anti-Predation Responses in a Superorganism

Insect societies are complex systems, displaying emergent properties much greater than the sum of their individual parts. As such, the concept of these societies as single ‘superorganisms’ is widely applied to describe their organisation and biology. Here, we test the applicability of this concept to the response of social insect colonies to predation during a vulnerable period of their life history. We used the model system of house-hunting behaviour in the ant Temnothorax albipennis. We show that removing individuals from directly within the nest causes an evacuation response, while removing ants at the periphery of scouting activity causes the colony to withdraw back into the nest. This suggests that colonies react differentially, but in a coordinated fashion, to these differing types of predation. Our findings lend support to the superorganism concept, as the whole society reacts much like a single organism would in response to attacks on different parts of its body. The implication of this is that a collective reaction to the location of worker loss within insect colonies is key to avoiding further harm, much in the same way that the nervous systems of individuals facilitate the avoidance of localised damage.     

The significance of multiple mating in the social wasp Vespula maculifrons

The evolution of the complex societies displayed by social insects depended partly on high relatedness among interacting group members. Therefore, behaviors that depress group relatedness, such as multiple mating by reproductive females (polyandry), are unexpected in social insects. Nevertheless, the queens of several social insect species mate multiply, suggesting that polyandry provides some benefits that counteract the costs. However, few studies have obtained evidence for links between rates of polyandry and fitness in naturally occurring social insect populations. We investigated if polyandry was beneficial in the social wasp Vespula maculifrons. We used genetic markers to estimate queen mate number in V. maculifrons colonies and assessed colony fitness by counting the number of cells that colonies produced. Our results indicated that queen mate number was directly, strongly, and significantly correlated with the number of queen cells produced by colonies. Because V. maculifrons queens are necessarily reared in queen cells, our results demonstrate that high levels of polyandry are associated with colonies capable of producing many new queens. These data are consistent with the explanation that polyandry is adaptive in V. maculifrons because it provides a fitness advantage to queens. Our research may provide a rare example of an association between polyandry and fitness in a natural social insect population and help explain why queens in this taxon mate multiply.     

Mating success and oviposition of a butterfly are not affected by non-lethal tissue sampling

Non-lethal methods of tissue sampling are increasingly used for genetic studies of insect species and the effects of this approach have long been assumed to be minimal. Tissue removal has the potential to influence insect reproductive behaviours such as mate recognition, courtship or oviposition but the effects of non-lethal sampling on reproductive success have not been widely and adequately tested. Here, we test potential effects of both wing-clipping and leg removal on reproductive behaviours of the cabbage white butterfly (Pieris rapae). We conducted a total of 93 male and 59 female mating trials, and found no significant differences in mating success between treated (i.e., tissue removed) and control individuals in either sex. We also monitored the number and location of eggs laid by 58 females. We found no significant differences in egg-laying behaviour among leg removed and control individuals. Power analysis indicated that we had sufficient statistical power to detect moderate effects of treatment on both mating and oviposition. Our study provides the most comprehensive examination to date of the effects of non-lethal sampling on reproductive behaviours in a butterfly/insect species, and supports the contention that tissue sampling is non-detrimental. To fully comprehend the general impacts of tissue sampling on butterfly reproductive behaviour however, additional similar studies need to be conducted on a variety of species with differing mating behaviours. Only through meta-analysis, may it be possible to detect more subtle effects of tissue removal which cannot be revealed within a single study due to sample size limitations.     

Reproductives and eggs trigger worker vibration in a subterranean termite

In insect societies, the presence of reproductives or eggs has been shown to shape several biological traits in the colony members. Social interactions are one of these traits that involve modification of the communication system of the entire colony. Many studies described the role of chemical compounds and dominance behaviors in the presence of reproductive but vibratory behaviors received very few investigations. Yet, vibratory behaviors are ideal candidates, particularly for subterranean species like termites, as they could be quickly transmitted through the substrate and could be very diversified (origin, modulation). Here, we investigated whether the presence of reproductives/eggs affects the vibratory behavior (body‐shaking) of workers in the subterranean termite Reticulitermes flavipes. Our results reveal that the presence of reproductives or eggs triggers an increase of workers' body‐shaking, independent of their colony of origin after 24 hr. We hypothesize that vibratory communication could be used to transfer information about the presence of reproductives and eggs to the entire colony, suggesting that vibratory behaviors could serve as an important yet neglected mediator of social regulation.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

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).