Evolution of eusociality

The evolution of eusociality occurred repeatedly in different orders of animals, particularly the hymenoptera. This 'true sociality' in animals, in which sterile individuals work to further the reproductive success of others, is found in termites, ambrosia beetles, gall-dwelling aphids, thrips, marine sponge-dwelling shrimp (Synalpheus regalis), naked mole-rats (Heterocephalus glaber), and nearly all Hymenoptera (which includes bees, wasps, and ants); that it should have evolved so many times in the hymenoptera, but remain rare throughout the rest of the animal kingdom, has made the evolution of eusociality a topic of debate among evolutionary biologists. Eusocial organisms at first appear to behave in stark contrast with simple interpretations of Darwinian evolution: passing on one’s genes to the next generation, or fitness, is a central idea in evolutionary biology.

Current theories propose that the evolution of eusociality occurred either due to kin selection, proposed by W.D. Hamilton, or by the competing theory of multilevel selection as proposed by E.O. Wilson and colleagues. No single trait or model is sufficient to explain the evolution of eusociality, and most likely the pathway to eusociality involved a combination of the pre-conditions, ecological factors, and genetic influences.

Overview of eusociality
Eusociality can be characterized by four main criteria: overlapping generations, cooperative brood care, philopatry, and reproductive altruism. Overlapping generations means that multiple generations live together, and that older offspring may help the parents raise their siblings. Cooperative brood care is when individuals other than the parents assist in raising the offspring through means such as food gathering and protection. Philopatry is when individuals remain living in their birthplace.

The final category, reproductive altruism, is the most divergent from other social orders. Altruism occurs when an individual performs a behavior that benefits a recipient in some way, but at the individual’s own expense. Reproductive altruism is one of the most extreme forms of altruism. This is when most members of the group give up their own breeding opportunities in order to participate in the reproductive success of other individuals. The individuals giving up their own reproductive success form a sterile caste of workers within the group. So far, each species that practices reproductive altruism is ruled by a queen, the only breeding female who is larger than the rest. The remainder of the society is composed of a few breeding males, sterile male and female workers, and the young.

Early hypotheses
Imagining the conditions in which eusociality could have evolved proved to be a problem for Darwin. In The Origin of Species, he described the existence of sterile worker castes in the social insects as "the one special difficulty, which at first appeared to me insuperable and actually fatal to my whole theory". In the next paragraph of his book, Darwin describes a solution. If the trait of sterility can be carried by some individuals without expression and those individuals that do express sterility help reproductive relatives, the sterile trait can persist and evolve.

Darwin was on the right track, except there is no sterile trait in these animals. The sterile workers are not actually physiologically sterile. Male workers can still produce sperm, and female workers sometimes lay eggs (observed in Hymenoptera, termites, and shrimp). And when the queen dies, one of the sterile females will become the new queen, obviously becoming capable of reproducing. The workers remain sterile through manipulation by the queen.

This insight led to Inclusive fitness and Kin selection becoming important theories during the 20th century to help explain eusociality. Inclusive fitness is described as a combination of one’s own reproductive success and the reproductive success of others that share similar genes. Animals may increase their inclusive fitness through kin selection. Kin selection is when individuals help close relatives with their reproduction process, seemingly because relatives will propagate some of the individual’s own genes. Kin selection follows Hamilton's Rule, which suggests that if the benefit of a behavior to a recipient, taking into account the genetic relatedness of the recipient to the altruist, outweighs the costs of the behavior to the altruist, then it is in the altruist's genetic advantage to perform the altruistic behavior.

Haplodiploidy/Kin selection
William D. Hamilton proposed that eusociality arose in social Hymenoptera by kin selection because of their interesting genetic sex determination trait of haplodiploidy. Because males are produced by parthenogenesis (they come from unfertilized eggs and thus only have one set of chromosomes), and females are produced from fertilized eggs, sisters share 75% of their genes, whereas mothers share only 50% of their genes with their daughters. Thus, sisters will propagate their own genes more by helping their mothers to raise more sisters, than to leave the nest and raise their own daughters. Though Hamilton's argument appears to work nicely for Hymenoptera, it excludes all other eusocial organisms, which are diploid (both males and females arise from eggs fertilized). Furthermore not all haplodiploid animals, such as many crabs and other arthropods, form eusocial societies. Other problems with this theory are when there are multiple males breeding with the queen because then siblings are less related. Also, male and female workers help raise the young, even though brothers and sisters only share 1/4 of their genes, which propagates an individual's genes less than normal sexual reproduction.

Inbreeding hypothesis
In species where philopatry predominates, and there are few emigrants to the nest, intense inbreeding can occur, as is the case in eusocial species. Inbreeding can mimic and even surpass the effects of haplodiploidy. Siblings may actually share greater than 75% of their genes. Like in haplodiploidy kin selection, the individuals can propagate their own genes more through the promotion of more siblings, rather than their own offspring.

Termite hypotheses
In termites, two additional hypotheses have been proposed. The first is called the Chromosomal Linkage Hypothesis, where a large part of the termite genome is sex-linked. This makes sisters related somewhat above 50%, and brothers somewhat above 50%, but brother-sister relatedness less than 50%. Termite workers might then bias their cooperative brood care towards their own sex. This hypothesis also mimics the effects of haplodiploidy, but proposes that males would help raise only the queen's male offspring, while females would only care for the queen's female offspring.

The symbiont hypothesis in termites is quite different from the others. With each molt, termites lose the lining of their hindgut and the subsequent bacteria and protozoa that colonize their guts for cellulose digestion. They depend on interactions with other termites for their gut to be recolonized, thus forcing them to become social. This could be a precursor, or pre-condition for why eusociality evolved in termites.

Pre-conditions
Although the symbiont hypothesis serves as a pre-condition for termites evolving into eusocial societies, scientists have found two crucial pre-conditions for the evolution of eusociality across all species. These include: 1. Altricial offspring (require large amounts of parental care to reach maturity); 2. Low reproductive success rates of solitary pairs that attempt to reproduce. These pre-conditions led to the two lifestyle characteristics that are observed in all eusocial species: nest building and extensive parental care.

Ecological factors
Ecological factors based on each species' food sources were also probably a precursor to eusociality. For example, the sponge-dwelling shrimp depend upon the sponge's feeding current for food, termites depend upon dead, decaying wood, and naked mole rats depend upon tubers in the ground. Each of these resources has patchy distributions throughout the environments of these animals. This means there is a high cost to dispersing (individual may not find another source before it starves), and these resources must be defended for the group to survive. These requirements make it a necessity to have high social order for the survival of the group.

Manipulation
Eusociality appears to be maintained through manipulation of the sterile workers by the queen. The mechanisms for this include hormonal control through pheromones, restricting food to young in order to control their size, consumption of any eggs laid by females other than the queen, and behavioral dominance. In naked mole rats, this behavioral dominance occurs in the form of the queen facing the worker head-to-head, and shoving it throughout the tunnels of the naked mole rats' burrow for quite a distance.

Model for the evolution of eusociality
Nowak, et al. (2010) outlines a path by which eusociality could evolve by means of multi-level selection in five steps:
 * 1) Formation of groups: Groups could consist of parent-offspring groups or unrelated groups (in situations where cooperation is beneficial) living in a structured nest.
 * 2) Pre-adaptations: Pre-adaptations for social living, such as progressive provisioning, will push the group further toward eusociality.
 * 3) Mutations: Mutations will arise and be selected. Some genes are known to have been silenced in social insect history, leading to the reduction of dispersal behavior and the origin of the wingless caste.
 * 4) Natural Selection Acts on Emergent Traits: The interactions of the individuals can be considered as part of the extended phenotype of the queen. These interactions produce emergent properties upon which natural selection can act.
 * 5) Multi-level selection: More cooperative groups out-compete less cooperative groups.