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Science. 1976 Jan 23;191(4224):249-63.

Haploidploidy and the evolution of the social insect.

Abstract

Halminton (1) was apparently the first to appreciate that the synthesis of Mendelian genetics with Darwin's theory of natural selection had profound implications for social theory. In particular, insofar as almost all social behavior is either selfish or altruistic (or has such effects), genetical reasoning suggests that an individual's social behavior should be adjusted to his or her degree of relatedness, r, to all individuals affected by the behavior. We call this theory kinship theory. The social insects provide a critical test of Hamilton's kinship theory. When such theory is combined with the sex ratio theory of Fisher (9), a body of consistent predictions emerges regarding the haplodiploid Hymenoptera. The evolution of female workers helping their mother reproduce is more likely in the Hymenoptera than in diploid groups, provided that such workers lay some of the male-producing eggs or bias the ratio of investment toward reproductive females. Once eusocial colonies appear, certain biases by sex in these colonies are expected to evolve. In general, but especially in eusocial ants, the ratio of investment should be biased in favor of females, and in it is expected to equilibrate at 1 : 3 (male to female). We present evidence from 20 species that the ratio of investment in monogynous ants is, indeed, about 1 : 3, and we subject this discovery to a series of tests. As expected, the slave-making ants produce a ratio of investment of 1 : 1, polygynoys ants produce many more males than expected on the basis of relative dry weight alone, solitary bees and wasps produce a ratio of investment near 1 : 1 (and no greater than 1 : 2), and the social bumblebees produce ratios of investment between 1 : 1 and 1 : 3. In addition, sex ratios in monogynous ants and in trapnested wasps are, as predicted by Fisher, inversely related to the relative cost in these species of producing a male instead of a female. Taken together, these data provide quantitative evidence in support of kinship theory, sex ratio theory, the assumption that the offspring is capable of acting counter to its parents' best interests, and the supposition that haplodiploidy has played a unique role in the evolution of the social insects. Finally, we outline a theory for the evolution of worker-queen conflict, a theory which explains the queen's advantage in competition over male-producing workers and the workers' advantage regarding the ratio of investment. The theory uses the asymmetries of haplodiploidy to explain how the evolved outcome of parent-offspring conflict in the social Hymenoptera is expected to be a function of certain social and life history parameters.

PMID:
1108197
[PubMed - indexed for MEDLINE]
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