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J Theor Biol. 1990 Jun 21;144(4):429-43.

Parasite diversity and the evolution of diploidy, multicellularity and anisogamy.

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A.B.R.G., Department of Zoology, Oxford, U.K.


It may be reasonably assumed that a diversity of parasite genotypes in any one cell or organism is more harmful than a population of uniform genotypes. If this is accepted the following consequences follow: (i) Parasite mixing, due to cytoplasm mixing, at the time of zygote formation is a new and additional cost of sex. The rapid divisions typical of zygotic cleavage may be viewed as an adaptation to minimize the degree of mixing of parasites in each daughter cell. The faster the divisions the less chance parasite populations have to grow and mix. Mitosis is the fastest form of cell division. Prolongation of the diploid phase follows as a consequence of mitosis in a diploid zygote. This view is unusual in that it demands no advantage per se to the possession of two chromosome sets. (ii) The cells of the blastula formed from rapid zygotic divisions are different as regards their symbiotic inclusions. If the right to gametogenesis is restricted, then every replicator symbiont and nuclear genome alike and hence every cell of the developing embryo, will have an incentive to compete. Selection between the clonal blastula cells would result in the cells of low parasite diversity forming the gametes. Thus, germ line restriction is in the interests of the nuclear genome. Controlling the right to gametogenesis is only possible if the blastula remains intact. Hence, multicellularity might have evolved so as to enable the limitation of the right to gametogenesis and hence reduce the parasite diversity of gametes. Inter-cell competition during embryogenesis is central to Buss's seminal notion of the evolution of developmental complexity within the metazoa. The above theory provides the missing motive force behind such competition. (iii) For a given zygote size, the fittest zygotes are those produced by the gametes most disparate in size because these have a lower diversity of parasites. This may be the advantage of anisogamy. The novelty of this new view of anisogamy is that it puts a premium on sperm being very small, in order to exclude parasites from sperm cytoplasm. The hypothesis is briefly tested by examining if there are alternative means of parasite limitation in organisms with large gametes.

[Indexed for MEDLINE]

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