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. 2009 Nov 12;364(1533):3169-79.
doi: 10.1098/rstb.2009.0129.

The Evolution of Extreme Altruism and Inequality in Insect Societies

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Free PMC article

The Evolution of Extreme Altruism and Inequality in Insect Societies

Francis L W Ratnieks et al. Philos Trans R Soc Lond B Biol Sci. .
Free PMC article

Abstract

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via 'voluntary altruism'. 'Enforced altruism' is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual's life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by 'policing', in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to 'acquiesce' to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.

Figures

Figure 1.
Figure 1.
Working versus reproducing. (a) In insect societies with morphologically distinct queens and workers, a female makes two life history decisions that determine whether it will reproduce or work. (b) In the honeybee, A. mellifera, owing to social coercion, most females become altruists at both these decision points. (c) In the honeybee, a species with low relatedness (r = 0.3) among female offspring owing to multiple mating by the mother queen, the proportions becoming altruists are much higher than expected based on ‘voluntary’ altruism alone, as would occur in the absence of coercion. (d) Individuals acquiesce to coercion by becoming altruists because they rear kin and so gain inclusive fitness. Worker honeybees are related to the queen's female and male offspring (r = 0.3, 0.25) even though this is not as high as the relatedness of a queen or an egg-laying worker to its own offspring (r = 0.5).
Figure 2.
Figure 2.
Direct and indirect effects on the level of altruism in a social group, as affected by kinship and relatedness. Kinship has a direct effect (voluntary altruism) but also a wide range of indirect effects via its effect on coercion (enforced altruism). In applying inclusive fitness theory, it is necessary to integrate these multiple effects. See table 1 and the text for examples of indirect effects.
Figure 3.
Figure 3.
How relatedness and coercion interact in the evolution of insect societies. At the origin of eusociality, relatedness is high but coercion is low or non-existent. As eusociality evolves further, the role of coercion and acquiescence increases and workers become morphologically distinct from queens. This allows relatedness to decrease via multiple mating by queens and/or polygyny. Extreme polygyny, as in some ants which are shown without wings, can cause relatedness to drop almost to zero. This may be an evolutionary dead end.

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