C

Cooperation in Social Consider a honey bee colony – perhaps the best known society (Winston 1987; Seeley Raghavendra Gadagkar 2010;Page2013). Their colonies comprise tens Centre for Ecological Sciences, of thousands of individual bees, among which Indian Institute of Science, Bangalore, India there is a single, large, and fertile female bee who is called the queen. Only the queen is mated, and with a store of sperm gathered Many of insects, such as ants, bees, from many males during her nuptial flight at wasps and termites, organize themselves into the beginning of her life, she can lay thousands societies that parallel, and sometimes better, of eggs per day, both fertilized eggs that develop human societies. They have impressive levels of into females and unfertilized eggs that develop social organization, communication, division into males. Colonies may comprise a few male of labor, cooperation and conflict, altruism and bees, also known as drones. The proverbially lazy self-sacrifice, policing and punishment, and drones do not take part in social life and do not learning and teaching. They can accomplish contribute to domestic work. Instead, they leave feats in warfare with neighboring colonies or their nests of birth and attempt to mate with virgin feats of internal cooperation such as the construc- queens of other colonies. Drones successful in tion of sophisticated nests or mounds, which mating die in the act of copulation as their genitals are impossible for individual colony members. are severed from their bodies and left hanging They are organized into colonies whose sizes onto the females. The rest of the colony comprises range from a few individuals up to a million smaller nearly sterile female bees, called workers. or more, occupying from a few centimeters to Workers have lost their genitalia over evolution- hundreds of square kilometers (Fig. 1). ary time and cannot mate and cannot produce

© Springer Nature Switzerland AG 2020 T. K. Shackelford, V. A. Weekes-Shackelford (eds.), Encyclopedia of Evolutionary Psychological Science, https://doi.org/10.1007/978-3-319-16999-6_1367-1 2 Cooperation in Social Insects

Cooperation in Social Insects, Fig. 1 Examples of the marginata; lower right, the tropical major eusocial insects. Upper left, the tropical weaver ant, mound-building termite (Odontotermes obesus). (Photos Oecophylla smaragdina; upper right, the Asian dwarf courtesy Dr. Thresiamma Varghese) honey bee Apis florea; lower left, the best studied Indian female offspring. They have small ovaries (much orderly, systematic fashion through a process smaller than those of the queen), but these usually known as age polyethism. Young bees begin by remain undeveloped in the queen’s presence. cleaning the nest, after which they successively Only upon the death of the queen and the colony transition to perform the tasks of building the nest, not being able to rear a new queen do some feeding the larvae, guarding the nest, and finally workers develop their ovaries and lay a few hap- venturing out to forage for pollen and nectar, loid, male-destined eggs. In the presence of a which serve as the sources of protein and carbo- healthy queen, workers refrain from reproduction hydrate, respectively, for the growing larvae. The and spend their whole lives working for the wel- task a bee performs depends on its relative age in fare of their colonies. Various tasks required for the colony. At the age at which they build the the functioning of the colony are performed in an nest, they have active wax glands that convert Cooperation in Social Insects 3 the nectar consumed into wax, which is used specific information about the distance and direc- for building the nest. As the worker bees get tion of the food source. Bees estimate the distance older, these wax glands degenerate, and their and direction of the food source by the image hypopharyngeal glands develop instead, secret- motion on their eyes of the surrounding landscape ing, many substances that are added to the diet (optic flow) and a process of dead reckoning of the larvae. Such relative age-based polyethism called path integration, keeping track of their has a built-in flexibility permitting the colony to successive linear and angular displacements as adaptively respond to unexpected changes they meander on their outward search flights in demography. Upon experimental removal of (Wehner 1992, Mandal 2018). Worker bees thus old bees, the relatively older of the intranidal devote their whole lives to the welfare of their workers becomes precocious foragers, leaving colony and do not reproduce, even in the form the nest at an abnormally younger absolute of a few male-destined eggs that they can poten- age than expected in normal colonies. tially lay. This is an extreme level of cooperation Conversely, upon experimental removal of that we label as altruism. Even more impressive young bees, the youngest of the foragers is their readiness to sting any marauder of their become over-aged nurses, reverting to nursing, nest, an act that leads to their immediate death, regenerating their already atrophied hypo- as they cannot withdraw their stings from pharyngeal glands. the bodies of their victims, owing to its outward- Division of labor is also modulated by the pointing barbs. spatial distribution of tasks, and of the bees, While there are some 10 species of honey bees and by their relative sensitivities of to the cues worldwide, all belonging to the genus Apis, signaling the need to perform certain tasks. in the family Apidae, there are at least 15,000 Queens mate with several males and produce species of ants, all belonging to the family daughters of several patrilines, contributing to Formicidae, found everywhere except in the the variability in the sensitivities of the bees to Arctic and Antarctic poles. The ants have reached perform different tasks. For instance, bees differ comparable levels of social complexity. Their in their response thresholds to the smell of dead species diversity permits the ants to embrace bees so that undertaker bees are those that are many lifestyles (Hölldobler and Wilson 1990). most sensitive to the smell. If a colony is For instance, leaf-cutting ants practice a missing the most sensitive patriline, however, sophisticated form of agriculture, cultivating the intensity of the smell will soon be adequate fungi in their gardens and feeding a population for another patriline to remove the dead bees. of up to a million or more individuals only with Sources of pollen and nectar are located by the products of their labor – fungal spores. some foragers, acting as scout bees; successful Medium-sized workers go out, locate, cut, and scouts return to the hive and recruit naïve bees to transport leaves back to their nests. These pieces transport the pollen or nectar back to the hive. of leaves of carefully chosen species are then This they do by the well-known honey bee ground into a fine paste and spread in the garden dance language. When the source is nearby, they by even smaller workers. Fungal mycelia are then perform a round dance motivating the bees to “planted” in the garden, and the spores eventually search nearby for the flowers with the expected harvested. The fungi cultivated – certain kinds of smell. When the source is more than about 500 m, mushrooms – are not known to exist outside the they perform a waggle dance, communicating fungal gardens of the ants. Certain cultivars of the 4 Cooperation in Social Insects fungi appear to have been selected and passed the gamergate. Diacamma genus presents a down across generations of ant colonies and occa- unique method of reproductive regulation, leading sionally exchanged between colonies. The ants to monogamy, i.e., reproductive monopoly by one have elaborate adaptations for manuring their gar- egg-laying individual. dens with their feces and for keeping out weeds, All social wasps are paper wasps because with the help of a cocktail of antibiotics produced they construct their nests not with wax as honey by bacteria they harbor on their own bodies. bees do, not with leaves as some ants do, and In contrast, weaver ants dwell in nests on trees not with soil as termites do but with paper. built by stitching leaves together with silk threads. They manufacture their own paper by scraping While hundreds of ants use their combined effort cellulose fibers from plants, adding their own to bend and maneuver leaves in alignment, some secretions to make a pulp and drying it. All social of them squeeze well-grown larvae to persuade wasps belong to the family . There them to donate some of their silk for the commu- is a very wide variation in the level of social nity good. Such donation of silk normally meant evolution within the Vespidae. Species belonging for their own pupation is costly to the larvae and to the subfamily Vespinae display advanced constitutes an act of altruism even before the sociality resembling the honey bees, while species individual becomes an adult. Reminiscent of the belonging to the subfamily Stenogastrinae are lazy drones in honey bees, male ant larvae socially very primitive, bordering on the solitary. are less likely to contribute silk for nest The subfamily are intermediate and building. Weaver ants are voracious predators in are considered primitively eusocial (see below). the tropical habitats of Africa (Oecophylla Their queens and workers are not morphologi- longinoda) and Asia (Oecophylla smaragdina) cally differentiated, and most adults eclose being and build interconnected series of nests across capable of taking on both queen and worker roles. several trees, with a single queen producing all Polistine wasps have been especially useful in the eggs required to maintain their colony investigating the evolution of social behavior populations. because they display the transition from solitary In even greater contrast, ants of the genus to social life within the lifetime of individual Diacamma in Asia have permanently lost their wasps. New polistine wasp nests may be founded queens. Their relatively small colonies (of a few by a single-mated female who can, much like a hundred individuals) consist only of workers, one solitary insect, build and guard her nest, lay of whom is mated and functions as a gamergate eggs, forage, and bring her offspring to adulthood, (mated worker) and lays all the eggs for all by herself. Her daughters from the first brood their colony. All workers are born with a pair of often stay back as sterile workers and assist her in wing buds called gemmae, which appear to be producing more offspring, making the nest now a necessary for the female ants to attract males. social unit. New nests may also be founded by The gamergate physically mutilates the gemmae small groups of females, in which case they are of all eclosing workers and thus prevents them social units from the start. Female wasps from mating and becoming reproductive. If the may function as workers for some time and gamergate dies, the next worker to eclose retains then transition to a queen status by leaving their her gemmae, becomes a gamergate, and mutilates parent nests and starting new single foundress all those who eclose after her. Mutilated workers nests and new multiple foundress nests as their perform all the tasks such as nest building, brood queens or may replace the queens of their parental care, and foraging, required to rear the brood of nests. These transitions permit us to study Cooperation in Social Insects 5 the costs and benefits of solitary as well as social only one or a few individuals in the colony repro- life and understand the ecological forces that mold duce, called queens or kings as the case may be, the evolution of social behavior, despite the cost while the rest function as sterile helpers, often of non-reproduction (Gadagkar 2001). called workers. Among the eusocial species, it is Termites represent the fourth main group of customary to recognize two further sub-divisions, insect societies. They are rather different in namely, the primitively eusocial and the advanced many ways. First, they do not belong to the insect or highly eusocial. Until the 1970s, order like the ants, bees, and wasps was thought to be restricted to ants, bees, and but belong to a different insect order, the Isoptera. wasps in the insect order Hymenoptera and Second, unlike the Hymenopteran social insects termites in the order Isoptera. In the last few which are haplodiploid (see below), they are dip- decades, eusociality has also been discovered in loid. They have both queens and kings that live thrips in the order Thysanoptera, aphids in the together as a monogamous pair. Their workers are order Hemiptera, ambrosia beetles in the order also of both sexes. In some species, the immature Coleoptera, and shrimps, in the class nymphs serve as workers and never complete their Crustacea. Barring the case of the naked mole metamorphosis into adults. Workers ingest plant rat that lives in underground tunnels in Africa material, digest the cellulose with the help of which curiously fits the definition, eusociality is gut microbiota, and feed the larvae and even restricted to insects and some shrimps. Despite the adult soldiers by regurgitating food to them this taxonomic range expansion of eusociality, by a process known as trophallaxis (Korb and advanced eusociality is restricted to ants, bees, Thorne 2017). wasps, and termites (Hölldobler and Wilson High levels of cooperation have made the 1990; Gadagkar 2001; Rubenstein and Abbot social insects ecologically successful – in some 2017). tropical forest habitats, social insects, especially, Biologists ask two kinds of questions about termites and ants, may constitute three-quarters of biological traits, the so-called proximate ques- the biomass. Biologists often use the terms tions (sometimes called “how” questions) and cooperation and altruism interchangeably. In ultimate questions (sometimes called “why” ques- both cases, the reference is to behavior costly for tions). In the context of cooperation in social the actor and beneficial to the recipient. As insects, examples of the proximate kind include described above, social insects are replete with questions such as how do social insects recognize examples of such costly cooperation. However, nestmates versus non-nestmates and maintain col- their levels of social integration and division of ony integrity; how do they divide colony labor labor vary greatly between different species among themselves; how does each member of so that they may be labelled as communal, the colony know what work to do when, and quasi-social, para-social, semi-social, sub-social, what not to do, so that they can function as an or eusocial (Wilson 1971). The last label, “euso- effective group; and how do they accomplish cial,” is considered the pinnacle of the evolution complex group tasks such as building elaborate of social complexity. Eusocial species exhibit nests, of locating, bringing, and processing food; (i) cooperative brood care, so that individuals etc. There is one overarching ultimate question, routinely care for offspring not their own; namely, how does natural selection favor the (ii) overlap of generations, so that caregivers evolution of altruistic sterility by a process can be younger than those who receive care; that is supposed to bring about survival of the and (iii) reproductive division of labor, so that fittest (fitness being usually measured as the 6 Cooperation in Social Insects

may vary between the primitively and highly eusocial species. In primitively eusocial species, queens and workers are not morphologically differentiated. Queens and workers and sometimes even the sub-groups of workers that specialize in performing different tasks are referred to as castes. Caste differentiation in the highly eusocial species takes place in their early larval stages leading to the eclosion of differenti- ated adults that can no longer change their fate. In the primitively eusocial species, however, adults at eclosion are completely or nearly totipotent and can subsequently differentiate into queens or workers. Since the main difference between queens and workers is that of reproduc- tion versus sterility, caste differentiation in highly eusocial species is developmentally regulated, while in primitively eusocial species, it is socially regulated. In highly eusocial species, the starting point of such differentiation is differential nutri- tion between queen-destined larvae and worker- destined larvae. The difference in nutrition may be one of the quality of the food, as in the case of the honey bee where queen larvae are fed with a sugar-rich royal jelly, while workers’ larvae are fed with ordinary worker jelly. Or it may Cooperation in Social Insects, Fig. 2 Our current involve a difference in the quantity of food such understanding of the proximate mechanism of reproductive caste differentiation that better-fed larvae become queens and poorly fed larvae become workers. Either way, number of offspring)? This can be split up differential nutrition channels larvae into into several sub-questions such as why does alternate developmental pathways such that natural selection favor group living instead of better-nourished larvae produce more insulin- solitary living; why is the division of labor, like peptides, turn on vitellogenin synthesis, the partitioning of tasks between different individ- develop their ovaries, and become queens. uals, more efficient than each individual Conversely, poorly nourished individuals produce performing tasks independent of each other; and less insulin-like peptides, produce little or no how does natural selection produce elaborate vitellogenin, fail to develop their ovaries, and communications systems such as the dance lan- become sterile workers (Chandra et al. 2018) guage of honey bees, for example? (Gadagkar (Fig. 2). Further subdivision of workers into 1997). sub-castes can also be mediated by differential We now have a fairly sophisticated understand- nutrition. In primitively eusocial species where ing of the proximate mechanisms of social caste differentiation is socially regulated, behav- behavior and cooperation. These mechanisms ioral dominance-subordinate interactions Cooperation in Social Insects 7 modulate caste differentiation such that behavior- by the proportion of genes shared between the ally dominant individuals become egg-laying altruist and the recipient is greater than the cost queens and subordinate individuals become non- incurred by the altruist (Box 1). This formulation egg-laying workers. Further subdivision among of the solution to the paradox of altruism is known workers into intranidal workers (those who work by several names – inclusive fitness theory, inside the nest) versus extranidal workers (those Hamilton’s rule, or kin selection. There has who work outside the nest) can also be mediated been a great deal of effort to develop a sound by similar aggressive interactions such that the mathematical foundation of this theory and relatively more dominant individuals among the some (but not enough) effort to see if workers, work at home, and the least dominant actually behave as if they obey Hamilton’s rule. individuals work outside, foraging for food and Hamilton’s rule can guide empirical researchers building material required by the colony. in the field and in the laboratory to ask the Social insects accomplish many rather right questions and measure the right quantities. complex tasks both inside and outside their nests Nevertheless, very few studies have adequately that appear to be inconsistent with their small measured all three parameters in Hamilton’s brains and limited neural capacity. The secret of rule to pronounce a clear verdict on whether their success in achieving complex outcomes altruists always obey Hamilton’s rule or incommensurate with the cognitive capacities of whether they sometimes get away without individual insects is that they use a process of obeying the rule. The latter possibility suggests decentralized self-organization – large numbers that there may be other ways of solving the of individuals follow simple local rules, but altruism paradox. Selection at the level of there emerges a complex outcome due to their the individual and also at the level of the whole collective behavior. This is sometimes called colony (known as multilevel selection) is social intelligence and is the subject of intense sometimes considered as promising avenues investigations by interdisciplinary teams of biol- for future research (Gadau and Fewell 2009). ogists, physicists, and mathematicians (Camazine Meanwhile, the very validity of the inclusive et al. 2003). fitness approach is being questioned by some Understanding the ultimate causation of soci- prominent researchers, leading to a bitter ality, namely, the evolution by natural selection of controversy (Nowak et al. 2010). As a result, the cooperation and altruism, has been an even greater study of cooperation in insect societies has gained preoccupation of social insect researchers. The a new vibrant dynamism, attracting much interest paradox of altruism referred to above was largely from theoreticians and empiricists alike, well solved, at least in theory, by the realization that beyond the traditional social insect community. evolutionary fitness can be gained not only by Although many interesting phenomena have producing one’s own offspring but also by aiding been discovered and their evolutionary logic is the reproduction of genetic relatives. Indeed, one being worked out, many more phenomena can combine the two kinds of fitness, direct surely await discovery. The study of cooperation (through offspring production) and indirect in social insects is worthy of attention from (through aiding genetic relatives), in a simple practitioners of diverse disciplines, not only additive manner. The sum of these two kinds of physics, chemistry, mathematics, and engineering fitness is known as inclusive fitness. Hamilton’s in the natural sciences but also psychology, rule predicts that natural selection can promote sociology, political science, and related the evolution of altruistic behavior when the disciplines in the social sciences. benefit to the recipient of altruism multiplied 8 Cooperation in Social Insects

Box 1 Hamilton’s Rule

b.r > c or b/c > 1/r

b = benefit to the recipient

c = cost to the altruist

r = genetic relatedness between the recipient and the altruist

or

ni ri > no ro

ni = number of relatives reared

ri = relatedness to relatives

no = number of offspring reared

ro = relatedness to offspring

Hamilton’s rule defines the condition for the evolution of altruism. The upper forms of the inequality are useful to predict when an individual will be selected to sacrifice itself to help others. The lower form is useful to predict when a sterile individual who rears relatives will be selected over a fertile individual who rears its own offspring

References insulin signaling and the evolution of eusociality in ants. Science, 361, 398–402. Gadagkar, R. (1997). Survival strategies: Cooperation Camazine, S., Deneubourg, J.-L., Franks, N. R., and conflict in animal societies. Cambridge, Sneyd, J., Theraulaz, G., & Bonabeau, E. (2003). Self- MA/Hyderabad: Harvard University Press/Universities organization in biological systems. Princeton/Oxford: Press. Princeton University Press. Gadagkar, R. (2001). The social biology of Ropalidia Chandra, V., Fetter-Pruneda, I., Oxley, P. R., marginata: Toward understanding the evolution of Ritger, A. L., McKenzie, S. K., Libbrecht, R., & Eusociality. Cambridge, MA: Harvard University Kronauer, D. J. C. (2018). Social regulation of Press. Cooperation in Social Insects 9

Gadau, J., & Fewell, J. (Eds.). (2009). Organization of Nowak, M. A., Tarnita, C. E., & Wilson, E. O. (2010). insect societies – From genome to sociocomplexity. The evolution of eusociality. Nature, 466, 1057–1062. Cambridge, MA: Harvard University Press. https://doi.org/10.1038/nature09205. Hölldobler, B., & Wilson, E. O. (1990). The ants. Page, R. E., Jr. (2013). The spirit of the hive – The mech- Cambridge, MA: Belknap Press of Harvard University anisms of social evolution. Cambridge, MA: Harvard Press. University Press. Korb, B., & Thorne, B. (2017). Sociality in termites. Rubenstein, D. R., & Abbot, P. (Eds.). (2017). In D. R. Rubenstein & P. Abbot (Eds.), Comparative Comparative social evolution. New York: Cambridge social evolution (pp. 124–153). Cambridge: Cambridge University Press. University Press. Seeley, T. D. (2010). Honeybee democracy. Princeton/ Mandal, S. (2018). How do animals find their way Oxford: Princeton University Press. back home? A brief overview of homing behavior Wehner, R. (1992). . In F. Papi (Ed.), Animal with special reference to social Hymenoptera. Insectes homing (pp. 45–144). London: Chapman and Hall. Sociaux, 65, 521–536. https://doi.org/10.1007/s00040- Wilson, E. O. (1971). The insect societies. Cambridge, 018-0647-2. MA: Harvard University Press. Winston, M. L. (1987). The biology of the honey bee. Cambridge, MA: Harvard University Press.