Evolution of eusociality

Eusociality is used to describe a high level of order within a group of individuals of a species. The highly structured colonies of ants, bees, and wasps are the most famous cases of eusociality, though other examples exist (termite, naked mole rat, etc). Eusociality has evolved numerous times in the order Hymenoptera (ants, bees, and wasps), as well as a few times in other arthropod groups, and once in mammals. That it should have evolved so many times in Hymenoptera, and remain so rare throughout the rest of the Animal Kingdom, has made eusociality a topic of interest and debate to many. More striking still, is that eusocial organisms at first appear to behave in stark contrast with what Darwinian evolution predicts. The workers in most eusocial colonies are sterile, and rather than reproduce, they help take care of their mother and siblings. Why an individual would surrender her reproductive rights in a eusocial colony remains a hot topic of debate.

Contents

Early Hypotheses

Imagining the conditions in which eusociality could have evolved proved to be a problem for Charles Darwin. He described, in The Origin of Species 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." [1] 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.[1] Thus, a queen in a social insect colony carries but does not express the trait of sterility. Her sterile daughters help feed and maintain the queen and her brood, so the workers are essentially aiding in the maintenance of the sterile trait. Darwin illustrated that "A breed of cattle always yielding oxen [castrates] with extraordinary long horns could be slowly formed by carefully watching which individual bulls and cows, when matched produced oxen with the longest horns; and yet no one ox could ever have propagated its kind" [1].

Inclusive Fitness and Kin Selection

During the twentieth century, Inclusive fitness and kin selection became important theories explain many social behaviors in animals. Inclusive fitness describes how an individual's behavior affects the combination of an individual's direct fitness (the number of offspring it produces) and the fitness of other individuals with similar genes. Kin selection is a subset of inclusive fitness pertaining specifically to individuals related by descent, and epitomized by Hamilton's Rule. Hamilton's Rule states that:

rb > c \

where

Hamilton's Rule suggests that if the benefit of a behavior to a recipient, weighted by the relatedness 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.

R.A. Fisher described situations in which individuals could benefit from the success of its relatives. Aposematic coloration in poisonous caterpillars makes the caterpillars more conspicuous to predators and warns them of the caterpillar's poisonous taste. However, predators must learn to avoid these brightly colored caterpillars by tasting one early in life. Fisher explained how the genes of this first caterpillar can benefit by being eaten by a predator. If the caterpillars travel in sibling groups, the individual that gets eaten will teach the predator to avoid the sibling group and the individual's sacrifice will have saved the lives of its siblings [2]

J.B.S. Haldane revealed his early understanding of inclusive fitness by famously remarking that he would not lay down his life for his brother, but that he would for two brothers or eight cousins [3].

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 and females are produced from fertilized eggs, sisters are essentially 75% related to each other whereas mothers are only 50% related to their daughters. Thus, sisters will benefit more by helping their mothers to raise more sisters than to leave the nest and raise their own daughters [4]. Hamilton's proposal of the importance of haplodiploidy in the evolution of eusociality reigned supreme amongst the scientists who study social hymenoptera for the rest of the century.

Failures of the Kin Selection Argument

Though Hamilton's argument appears to work nicely for ants, bees, and wasps, it excludes eusocial organisms that are not haplodiploid. These organisms include the mammalian naked mole rat, aphids, thrips, brine shrimp, and a species of beetle (amongst some other examples) [5]. The most striking example is that of the social Isoptera, the termites which have highly sophisticated colonies but do not display haplodiploidy.

Hamilton's argument also does not take into account species that are haplodiploid but are not eusocial, such as solitary wasps and bees.

There also exist several cases of eusocial haplodiploid species that have decreased levels of relatedness so that sisters no longer share an average of 75% of their genes. This can be due to having multiple queens in the colony or by multiple matings by a queen prior to starting a colony [6].

The kin selection model may be too constrained to aptly describe the reality of a eusocial colony. It assumes that fitness can be described by additive isolated interactions and that these interactions are binary. However, social insects often benefit from cooperation between many individuals[7].

Group Selection

An alternative theory to kin selection is that eusociality evolved by group selection. While selection would still work on the gene level and the individual level, it would simultaneously act upon groups of individuals. Nowak, et al. (2010)[7] outline 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[8]

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.

Nowak, et al (2010) did not settle the debate over how eusociality evolved. Many researchers still argue that kin selection remains the best explanation [9][10].

References

  1. ^ a b c Darwin, C. (1859) On the Origin of Species by Means of Natural Selection or The Preservation of Favored Races in the Struggle for Life. Reprinted 1998, Modern Library; New York, NY.
  2. ^ Fisher, Ronald A. (1930) The Genetical Theory of Natural Selection. 2nd ed., 1958. New York: Dover.
  3. ^ Maynard Smith (1975) Personal comm.
  4. ^ Hamilton, W.D. (1964) The genetical theory of social behaviour, I,II. Journal of Theoretical Biology. 7:1-52
  5. ^ Costa, J.T. (2006) The Other Insect Societies. Belknap Press.
  6. ^ Holldobler, B. and Wilson, E. O. (1994) Journey to the Ants. Belknap Press.
  7. ^ a b Nowak, et al. (2010) The evolution of eusociality. Nature vol 466:26.
  8. ^ Abouheif, E. & Wray, G. A. Evolution of the gene network underlying wing polyphenism in ants. Science 297, 249–252 (2002).
  9. ^ Foster, K.R. et al (2005) Kin selection is the key to altruism. TRENDS in Ecology and Evolutionary Biology.
  10. ^ Queller, DC and Strassmann JE (1998) Kin selection and social insects. Bioscience, 48: 165-175