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Eusociality (Greek eu: "good/real" + "social"), the highest level of organization of animal sociality, is defined by the following characteristics: cooperative brood care (including brood care of offspring from other individuals), overlapping generations within a colony of adults, and a division of labor into reproductive and non-reproductive groups. The division of labor creates specialized behavioral groups within an animal society which are sometimes called castes. Eusociality is distinguished from all other social systems because individuals of at least one caste lose the ability to perform at least one behavior characteristic of individuals in another caste.

Eusociality is mostly observed and studied in Hymenoptera (ants, bees, wasps, and termites). For example, a colony has caste differences; a queen and king take the roles as the sole reproducers and the soldiers and workers work together to create a living situation favorable for the brood. In addition to Hymenoptera, there are two known eusocial vertebrates from the order Rodentia, which includes the naked mole rat and the Damaraland mole rat. Most of the individuals cooperatively care for the brood of a single reproductive female (the queen) to which they are most likely related to.

Several other levels of animal sociality have been distinguished. These include presocial (solitary but social), subsocial and parasocial (including communal, quasisocial, and semisocial).

History
The term "eusocial" was introduced in 1966 by Suzanne Batra who used it to describe nesting behavior in Halictine bees. Batra observed the cooperative behavior of the bees, males and females alike, as they took responsibility for at least one duty (i.e. burrowing, cell construction, oviposition) within the colony. The cooperativeness was essential as the activity of one labor division greatly influenced the activity of another. For example, the size of pollen balls, a source of food, depended on when the egg-laying females oviposited. If the provisioning by pollen collectors was incomplete by the time the egg-laying female occupied a cell and oviposited, the size of the pollen balls would be small, leading to small offspring.

In 1969, Charles D. Michener further expanded Batra’s classification with his comparative study of social behavior in bees. He observed multiple species of bees (Apoidea) in order to investigate the different levels of animal sociality, all of which are different stages that a colony may pass through. Eusociality, which is the highest level of animal sociality a species can attain, specifically had three characteristics that distinguished it from the other levels:


 * 1) “Egg-layers and worker-like individuals among adult females" (division of labor)
 * 2) The overlap of generations (mother and adult offspring)
 * 3) Cooperative work on the cells of the bees' honeycomb

Up to this point, “eusocial” was a term used to describe some of the cooperative living and brood caring carried out by bees. E. O. Wilson then extended the term to social insects aside from bees, such as ants, wasps, and termites. Originally, it was defined to include organisms (only invertebrates) that had the following three features:


 * 1) Reproductive division of labor (with or without sterile castes)
 * 2) Overlapping generations
 * 3) Cooperative care of young

As eusociality became a recognized widespread phenomenon, however, it was also discovered in Chordata, specifically Rodentia.

Further research also distinguished another possible important criterion for eusociality, known as “the point of no return”. This phenomenon is characterized by eusocial individuals that become fixed into one behavioral group, which usually occurs before reproductive maturity. This prevents them from transitioning between behavioral groups and creates an animal society that is truly dependent on each other for survival and reproductive success. For many insects, this irreversibility has changed the anatomy of the worker caste, which is sterile and provides support for the reproductive caste.

Examples
Most eusocial societies exist in arthropods, while few are found in mammals.

In Insects
The order Hymenoptera contains the largest group of eusocial insects, including ants, bees, and wasps – those with reproductive “queens” and more or less sterile “workers” and/or “soldiers” that perform specialized tasks. While only a small percentage of species in bees (family Apidae) and wasps (Sphecidae and Vespidae) are eusocial, nearly all species of ants (Formicidae) are eusocial. Polistes metricus and Polistes annularis are wasps that demonstrate eusocial behavior. An acrobat ant is an example of ant that shows eusocial behavior. Other examples of organisms that use the eusocial colony structure are Eciton burchellii, an army ant species, and red harvester ants. Eusociality in these families of organisms is likely managed by a set of pheromones that alter the behavior of specific castes in the colony. These pheromones may act across different species, as have been observed in Apis andreniformis (black dwarf honey bee), where worker bees were under the influence of queen pheromone from the related Apis florea (red dwarf honey bee). Such a phenomenon of reproductive specialization generally involves the production of sterile members of the species, which carry out specialized tasks to care for the reproductive members. It can manifest in the appearance of individuals within a group whose behavior or morphology is modified for group defense, including self-sacrificing behavior ("altruism"). An excellent example of a species whose sterile caste displays this altruistic behavior is Myrmecocystus mexicanus, or one of the species of honey ant. Select sterile workers fill their abdomens with liquid food until they become immobile and hang from the ceilings of the underground nests, acting as food storage for the rest of the colony.

Termites (order Isoptera) make up another large portion of highly advanced eusocial animals. The colony is differentiated into various castes: the queen and king are the sole reproducing individuals; workers forage and maintain food and resources; and soldiers defend the colony against ant attacks. The latter two castes, which are sterile and perform highly specialized, complex social behaviors, are derived from different stages of pluripotent larvae produced by the reproductive caste. Some soldiers have jaws so enlarged (specialized for defense and attack) that they are unable to feed for themselves and must be fed by workers.

Austroplatypus incompertus, a species of weevil native to Australia, is the first beetle (order Coleoptera) to be recognized as eusocial. Also known as the “ambrosia beetle,” this species forms colonies in which a single female is fertilized and protected by many unfertilized females which also serve as workers excavating tunnels in trees. The ambrosia beetle also participates in cooperative brood care, in which individuals care for juveniles that are not their own.

Recently, some species of gall-making aphids (order Hemiptera), including the gall-forming aphid, Pemphigus spyrothecae, and thrips (order Thysanoptera), small insects that live in and feed on plant tissue, were also found to be eusocial. These species have very high relatedness among individuals due to their partially asexual mode of reproduction (sterile soldier castes being clones of the reproducing female), but the gall-inhabiting behavior gives these species a defensible resource that sets them apart from related species with similar genetics. They produce soldier castes capable of fortress defense and protection of their colony against both predators and competitors. In these groups, therefore, high relatedness alone does not lead to the evolution of social behavior, but requires that groups occur in a restricted, shared area. These species have morphologically distinct soldier castes that defend against kleptoparasites (parasitism by theft) and are able to reproduce parthenogenetically (without fertilization).

In Crustaceans
Eusociality has also arisen among some crustaceans that live in groups in a restricted area. Synalpheus regalis, parasitic shrimp that rely on fortress defense and live in groups of closely related individuals in tropical reefs and sponges, live eusocially with a single breeding female and a large number of male defenders, armed with enlarged snapping claws. As with other eusocial societies, there is a single shared living space for the colony members, and the non-breeding members act to defend it.

In Mammals
Mammalian examples include the naked mole rat and the Damaraland mole rat (Heterocephalus glaber & Fukomys damarensis, respectively), two species of vertebrates that are diploid and highly inbred. Usually living in harsh or limiting environments, these mole rats aid in raising siblings and relatives born to a single reproductive queen. However, this classification is controversial owing to disputed definitions of 'eusociality.' A study conducted by O’Riain and Faulkes in 2008 suggests that due to regular inbreeding avoidance, mole rats sometimes outbreed and establish new colonies when resources are sufficient. Thus, it is uncertain whether mole rats classify as true eusocial organisms, since their social behavior depends largely on their resources and environment.

Phylogenetic Distribution of Eusociality
Eusociality is a rare but widespread phenomena originating in members of the seven aforementioned orders- Rodentia (mole rats), Decapoda (snapping shrimp), Thysanoptera (thrips), Hemiptera (aphids), Isoptera (termites), Coleoptera (ambrosia beetles), and Hymenoptera (ants, bees, and wasps). All species of termites are eusocial, and it is believed that they were the first eusocial animals to evolve, sometime in the upper Jurassic period (~150 million years ago). All other orders also contain non-eusocial species, including many lineages where eusociality was inferred to be the ancestral state. Thus the number of independent evolutions of eusociality is still under investigation.



The Paradox of Eusociality
Eusocial animals have appeared paradoxical to many theorists of the field of evolution: if adaptive evolution unfolds by differential survival of individuals, how can individuals incapable of passing on their genes possibly evolve and persist? In Origin of Species (first edition, Ch. 8), Darwin referred to the existence of sterile castes as the "one special difficulty, which at first appeared to me insuperable, and actually fatal to my theory." Darwin anticipated that a possible resolution to the paradox might lie in the close family relationship, which W.D. Hamilton would later quantify with his inclusive fitness theory.

Inclusive Fitness and Haplodiploidy
According to inclusive fitness theory, organisms can gain fitness not just through increasing their own reproductive output, but also via increasing the reproductive output of other individuals that share their genes, especially their close relatives. Individuals will be selected to help their relatives when the cost of helping is less than the benefit gained by their relative multiplied by the fraction of genes that they share, i.e. when Cost < relatedness * Benefit. Under inclusive fitness theory, the necessary conditions for eusociality to evolve are more easily fulfilled by haplodiploid species because of their unusual relatedness structure. In haplodiploid species, females develop from fertilized eggs and males develop from unfertilized eggs. Because a male is haploid, his daughters will share 100% of his genes and 50% of their mothers. Therefore, they will share 75% of their genes with each other. This mechanism of sex determination gives rise to what W. D. Hamilton first termed "supersisters" who are more related to their sisters than they would be to their own offspring. Even though workers often do not reproduce, they can potentially pass on more of their genes by helping to raise their sisters than they would by having their own offspring (each of which would only have 50% of their genes). This unusual situation where females may have greater fitness when they help rear siblings rather than producing offspring is often invoked to explain the multiple independent evolutions of eusociality (arising at least nine separate times) within the haplodiploid group Hymenoptera. However, now many eusocial species have been discovered that are not haplodiploid (including termites, some snapping shrimp, and mole rats). Conversely many bees are haplodiploid yet are not eusocial, and among eusocial species many queens mate with multiple males, thus resulting in a hive of half-sisters that only share 25% of their genes. The association between haplodiploidy and eusociality is below statistical significance, all of which suggests that haplodiploidy alone is neither necessary nor sufficient for eusociality to emerge. However relatedness does still play a part, as monogamy (queens mating singly) has been shown to be the ancestral state for all eusocial species so far investigated.

The Ecology of Eusociality
Many scientists citing the close phylogenetic relationships between eusocial and non-eusocial species are making the case that environmental factors are especially important in the evolution of eusociality. The relevant factors primarily involve the distribution of food and predators.

With the exception of some aphids, all eusocial species live in a communal nest which provides both shelter and access to food resources. Mole rats and ants live in underground burrows; wasps, bees, and some termites build above-ground hives; thrips and aphids inhabit galls (neoplastic outgrowths) induced on plants; ambrosia beetles and some termites nest together in dead wood; and snapping shrimp inhabit crevices in marine sponges. For many species the habitat outside the nest is often extremely arid or barren, creating such a high cost to dispersal that the chance to take over the colony following parental death is greater than the chance of dispersing to form a new colony. Defense of such fortresses from both predators and competitors often favors the evolution of non-reproductive soldier castes, while the high costs of nest construction and expansion favor non-reproductive worker castes.

The importance of ecology is supported by evidence such as experimentally induced reproductive division of labor, for example when normally solitary queens are forced together. Conversely, female Damarland mole rats undergo hormonal changes that promote dispersal after periods of high rainfall, supporting the plasticity of eusocial traits in response to environmental cues.

Multilevel Selection
Once pre-adaptations such as group formation, nest building, high cost of dispersal, and morphological variation are present, between-group competition has been cited as a quintessential force in the transition to advanced eusociality. Because the hallmarks of eusociality will produce an extremely altruistic society, such groups will out-reproduce their less cooperative competitors, eventually eliminating all non-eusocial groups from a species.

Multilevel selection has been heavily criticized by some for its conflict with the kin selection theory.

Physiological and Developmental Mechanisms of Eusociality
An understanding of the physiological causes and consequences of the eusocial condition has been somewhat slow; nonetheless, major advancements have been made in learning more about the mechanistic and developmental processes that lead to eusociality.

Involvement of Pheromones
Pheromones are thought to play an important role in the physiological mechanisms underlying the development and maintenance of eusociality. The most well-studied queen pheromone system in social insects is that of the honey bee Apis mellifera. Queen mandibular glands were found to produce a mixture of five compounds, three aliphatic and two aromatic, which have been found to control workers. Mandibular gland extracts inhibit workers from constructing queen cells in which new queens are reared which can delay the hormonally based behavioral development of workers and can suppress ovarian development in workers. Both behavioral effects mediated by the nervous system often leading to recognition of queens (releaser) and physiological effects on the reproductive and endocrine system (primer) are attributed to the same pheromones. These pheromones volatilize or are deactivated within thirty minutes, allowing workers to respond rapidly to the loss of their queen.

The levels of two of the aliphatic compounds increase rapidly in virgin queens within the first week after eclosion (emergence from the pupal case), which is consistent with their roles as sex attractants during the mating flight. It is only after a queen is mated and begins laying eggs, however, that the full blend of compounds is made. The physiological factors regulating reproductive development and pheromone production are unknown.

In several ant species, reproductive activity has also been associated with pheromone production by queens. In general, mated egg laying queens are attractive to workers whereas young winged virgin queens, which are not yet mated, elicit little or no response. However, very little is known about when pheromone production begins during the initiation of reproductive activity or about the physiological factors regulating either reproductive development or queen pheromone production in ants.

Among ants, the queen pheromone system of the fire ant Solenopsis invicta is particularly well studied. Both releaser and primer pheromones have been demonstrated in this species. A queen recognition (releaser) hormone is stored in the poison sac along with three other compounds. These compounds were reported to elicit a behavioral response from workers. Several primer effects have also been demonstrated. Pheromones initiate reproductive development in new winged females, called female sexuals. These chemicals also inhibit workers from rearing male and female sexuals, suppress egg production in other queens of multiple queen colonies and cause workers to execute excess queens. The action of these pheromones together maintains the eusocial phenotype which includes one queen supported by sterile workers and sexually active males (drones). In queenless colonies that lack such pheromones, winged females will quickly shed their wings, develop ovaries and lay eggs. These virgin replacement queens assume the role of the queen and even start to produce queen pheromones. There is also evidence that queen weaver ants Oecophylla longinoda have a variety of exocrine glands that produce pheromones, which prevent workers from laying reproductive eggs.

The mode of action of inhibitory pheromones which prevent the development of eggs in workers has been convincingly demonstrated in the bumble bee Bombus terrestris. In this species, pheromones suppress activity of the corpora allata and juvenile hormone (JH) secretion. The corpora allata is an endocrine gland that produces JH, a group of hormones that regulate many aspects of insect physiology. With low JH, eggs do not mature. Similar inhibitory effects of lowering JH were seen in halictine bees and polistine wasps, but not in honey bees.

Other Strategies
A variety of strategies in addition to the use of pheromones have evolved that give the queens of different species of social insects a measure of reproductive control over their nest mates. In many Polistes wasp colonies, monogamy is established soon after colony formation by physical dominance interactions among foundresses of the colony including biting, chasing and food soliciting. Such interactions created a dominance hierarchy headed by individuals with the greatest ovarian development. Larger, older individuals often have an advantage during the establishment of dominance hierarchies. The rank of subordinates is positively correlated with the degree of ovarian development and the highest ranking individual usually becomes queen if the established queen disappears. Workers do not oviposit when queens are present because of a variety of reasons: colonies tend to be small enough that queens can effectively dominate workers, queens practice selective oophagy or egg eating, or the flow of nutrients favors queen over workers and queens rapidly lay eggs in new or vacated cells.

In primitively eusocial bees (where castes are morphologically similar and colonies usually small and short-lived), queens frequently nudge their nest mates and then burrow back down into the nest. This behavior draws workers into the lower part of the nest where they may respond to stimuli for cell construction and maintenance. Being nudged by the queen may play a role in inhibiting ovarian development and this form of queen control is supplemented by oophagy of worker laid eggs. Furthermore, temporally discrete production of workers and gynes (actual or potential queens) can cause size dimorphisms between different castes as size is strongly influenced by the season during which the individual is reared. In many wasp species worker caste determination is characterized by a temporal pattern in which workers precede non-workers of the same generation. In some cases, for example in the bumble bee, queen control weakens late in the season and the ovaries of workers develop to an increasing extent. The queen attempts to maintain her dominance by aggressive behavior and by eating worker laid eggs; her aggression is often directed towards the worker with the greatest ovarian development.

In highly eusocial wasps (where castes are morphologically dissimilar), both the quantity and quality of food seem to be important for caste differentiation. Recent studies suggest that differential larval nourishment may be the environmental trigger for larval divergence into one of two developmental classes destined to become either a worker or a gyne. When larvae are nourished with royal jelly, which is secreted by workers, they differentiate into queens. This jelly seems to contain a specific protein, designated as royalactin, which increases body size, promotes ovary development and shortens the developmental time period. Furthermore, the differential expression in Polistes of larvae genes and proteins, also differentially expressed during queen versus caste development in honey bees, indicate that regulatory mechanisms may occur very early in development.

Definition Debates
Subsequent to Wilson's original definition, other authors have sought to narrow or expand the definition of eusociality by focusing on the nature and degree of the division of labor, which was not originally specified. A narrower and more widely accepted definition specifies the requirement for irreversibly distinct behavioral groups or castes (with respect to sterility and/or other features). Such a definition, however, excludes social vertebrates, like the mole rats, and some Hymenoptera species, like the weaver ants. For example, depending on the availability of resources and the condition of the environment, mole rats can change between different types of social behaviors. In 2005, according to Wilson and Holldöbler, these types of animals would be considered primitively eusocial, which is different from eusocial, since the labor division is not permanent. A broader definition, on the other hand, would include mole rats because it allows for any temporary division of labor or non-random distribution of reproductive success to constitute eusociality.

In 2010, Nowak, Tarnita and Wilson challenged the theoretical explanation of the evolution of eusociality. Based on the concept of inclusive fitness, the kin selection theory considers the relatedness of individuals to be one of the most important factors that lead to eusociality. This brought up issues like the irrelevance of haplodiploidy and maternal control. Nowak et al. argued that the kin selection theory is inadequate because it can explain only a subset of eusocial populations due to its assumptions (i.e. “all interactions must be additive and pairwise” which excludes any interaction that involves more than two players). To them, the standard natural selection theory, which is a more general approach than the current explanation of eusociality, is the appropriate theory to use since it explains the same phenomenon and it would work for a larger number of eusocial cases. It also requires simpler mathematical calculations when explaining the evolution of eusociality. This paper led to a large influx of publications that refuted Nowak et al.’s ideas and supported the validity and specificity of the kin selection theory. For example, Trivers and Hare studied the haplodiploid Hymenoptera and they found that the workers were able to win the parent-offspring conflict, countering the parents’ best interest and selecting the outcome that has the greater benefit for the workers (i.e. reproductive success with shares higher relatedness to workers than the queen). This refuted Nowak et al.’s defense that future offspring development could be based solely on the fitness of parents.

Another debate focused on whether or not humans may be considered eusocial. In Wilson's latest book, 2012's The Social Conquest of the Earth, he refers to humans as a species of eusocial ape. He supports his reasoning by stating our eusocial similarities to ants. Humans also fall under Wilson's original criteria of eusociality (division of labor, overlapping generations, and cooperative care of young including ones that are not their own). Through cooperation and teamwork, ants and humans gain a type of “superpower” that is unavailable to other social animals that have failed to make the leap from social to eusocial. Eusociality creates the superorganism. This has caused conflict amongst biologists as not all believe that a term reserved for invertebrates can explain humanity. Others do not believe that humans are eusocial because humans make the decision to be "cooperative" (i.e. babysitting a non-related child) whereas eusociality is a behavioral strategy that is not specifically selected by an individual.