Biology 441. Animal Behavior
Lecture 29. Wednesday, 11 December 1996

EUSOCIALITY IN INSECTS

Eusocial insects are characterized by 3 traits: (1) cooperative care of young by more individuals than just the mother, (2) sterile castes, and (3) overlap of generations so that the mother, adult offspring (usually sterile) and young offspring are all alive at the same time. Thus older sterile offspring aid their mother (or parents) in raising younger siblings. In many, but not all, eusocial insects there is also division of labor and caste differentiation among the sterile individuals (e.g., see handout). Eusociality occurs in 3 orders: Hymenoptera (all ants, some bees, wasps), Isoptera (termites) and Homoptera (rarely in aphids).

Termites

Termites are eusocial. They are in the order Isoptera and are related to cckroaches. They are diploid, and both sexes are equally involved in social behavior. The most important factor that probably favored the evolution of eusociality is the need to transmit symbiotic cellulose-digesting microorganisms between individuals after hatching and each molt (the wall of the gut is shed during each molt). Defense was probably also important factor in the evolution of eusociality--primitive termites have only one nonreproductive caste, the soldier. Soldiers and other nonreproductive castes are "neotenics", lacking the ability to reproduce.

David Barash and Peter Lenz formulated one potential model for the evolution of eusociality in termites (see handout). The first step likely depended on the necessity of transfer of anaerobic symbionts; thus, mothers would be selected to remain near their eggs and to transfer symbionts upon eclosion. Cellulose digestion permits safe residence within food sources, e.g., logs. A termite mother becomes larger as she feeds and can gain tremendously in egg-laying ability. For example, a queen Macrotermes natalensis can produce 36,000 eggs in a day.

A male is certainly more fit staying with a large egg-laying female than searching for a new mate. In present-day termites, matings are monogamous and the male and female remain together throughout their lives. Monogamy means that offspring are full siblings, further inclining nonreproductive castes to aid in he production of additional soldiers and workers and periodically in the production of sexual offspring (full siblings, r=0.5) of the king and queen. Queens are intolerant of reproduction (unless they are ready to produce young that will disperse and breed) and transmit sterility pheromones to female workers. Kings likewise inhibit reproductive development in males. Termite eusociality is explained largely by parental manipulation of young and perhaps the benefits of kin selection to the nonreproductive castes.

Hymenoptera

In the eusocial Hymenoptera a colony consists of reproductive females (queens) and sterile females (workers); males (drones) do not aid in the colony and are produced only when fertilization of new queens is about to occur. Typically, there is only one queen in the colony and the workers don't ever breed. There are exceptions, however, of both multiple queens and reproductive workers in some species. Because workers never mate, they can only produce male offspring (drones) from unfertilized eggs (see below) and cannot produce daughters.

Sex determination

W. D. Hamilton realized that a key to understanding eusociality in the Hymenoptera may lie in how sex is determined in this order. Unfertilized haploid eggs develop into males (drones); fertilized eggs develop into females (queens or workers). This sex determination system is called haplodiploidy. Among females, caste depends on the type of food provisioning of the larvae and has no genetic basis.

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A queen is diploid and the probability that she provides a particular allele to a son is 0.5. On the other hand, the son receives all of his genes from his mother (remember that he is haploid), therefore, the son's coefficient of relatedness to his mother is 1.0. Males don't have sons in this system.

Since males are haploid, all the sperm they produce will be identical. If a queen mates with only one male, all of her daughters will have an identical set of paternal genes. There is a 50% chance that a daughter and mother will share a maternal gene. Therefore, daughters of monogamous mothers have a coefficient of relatedness to their mother of 0.5, but they have a coefficient of relatedness to each other of 0.75 (1/2 of genes from mother and all of the genes from the father are identical -- see handout). Therefore, full sisters are more closely related to each other than they would be to their own daughters!

Ecological factors

Many bees and wasps are not eusocial, and some are primitively eusocial. In the paper wasp Polistes metricus sometimes queens solitarily establish nests and sometimes two sisters jointly establish nests. There is a clear dominance order between the sisters when they establish a nest jointly, and the dominant female does nearly all of the egg laying. Because 2 females are far better able to defend their nest against predators and parasites, even the subordinate female has higher inclusive fitness than do solitary females. Sharing nests may be one avenue to eusociality; eusociality also may have arisen through advantages of young remaining in the motherís nest (see handout).

Like termite queens, Hymenopteran queens are essentially egg-laying machines and have been called "super-reproductives". Perhaps by helping their mother reproduce, sterile workers benefit more through kin selection than they could benefit genetically by their own reproduction. Like the termites, however, queen suppression of reproduction in workers may be a key factor.

Michener and Brothers (1974. Proc. Nat. Acad. Sci. 71:671-674) studied a species of primitively eusocial bees, Lasioglossum zephyrum , and concluded that queens dominate the workers, inhibiting them from becoming queens. Queens have high activiy levels and nudge the workers in agonistic interactions (just like queen naked mole-rats do). Workers do not develop functional ovaries, and queens nudge the workers with the largest developing ovaries the most. Queens also eat worker-laid (drone) eggs. Queens constantly draw young workers back into the nest, keeping them there by force. Workers may benefit though kin selection because they would have a very low chance of successfully establishing their own nest.

Young colonies of the neotropical wasp, Metapolybia azecoides , contain a different type of females, mated egg-layers (subordinate queens) that produce workers but are forced out of the colony or become nonreproducing workers before producing queens or drones. These temporary queens resemble workers in that they make no genetic contributions to future generations, instead enhancing the development of the colony and the eventual reproductive success of the dominant queen. The subordinate queens are thought to be sisters of the dominant queen who dispersed from the natal colony with her.

Lin and Michener (1972. Q. Rev. Biol. 47:131-159) suggested that it is necessary to consider ecological factors closely when considering how sociality could have developed in the Hymenoptera. Examining the less social grades of bees and wasps, they found that much of the social behavior is mutualistic. The need for defense of the nest or hive is probably the initial reason for sociality beyond mating.

In many primitively social and even in some eusocial species, workers may be reproductive and may produce most, if not all, of the male offspring (drones). In primitively social bees, both queens and workers benefit from associating with each other, queens simply benefit more. It may be unnecessary to implicate kin selection in the evolution of sociality in the Hymenoptera until the evolutionary development of sterile castes. Even then, nonreproductive individuals may have little choice in the matter: queens may inhibit their sexual development. They are likely "making the best of a bad situation", helping a belligerent relative, their mother, produce related offspring.

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