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Every sexual species is potentially vulnerable to a wide range of heritable factors that disrupt the normal patterns of inheritance. Why these selfish elements are not more common is not well understood. Here, by reference to the dynamics of cytoplasmic incompatibility, we propose a novel solution, namely that under certain conditions, the most likely trajectory is for the selfish element to invade, followed by slow decay to complete loss. Cytoplasmic incompatibility is found in several arthropod species and is characterized by the fact that crosses between males infected with vertically transmitted bacteria of the genus Wolbachia and uninfected females produce significantly fewer adult progeny than the other mating combinations. Early models revealed that such bacteria are expected to spread very rapidly and persist at high frequencies. This being so, cytoplasmic incompatibility should be stably maintained through cladogenesis, thus most sub-populations within a species should be affected. Contrary to these expectations is the finding that cytoplasmic incompatibility within species is patchily distributed and rare. More recent analyses suggest that although Wolbachia should persist in populations the sterilizing effect may wane. We extend one of these analyses and find that through most parameter space, following the invasion of cytoplasmic incompatibility inducing Wolbachia into an uninfected population, not only will the sterilizing effect wane but the conditions become permissive for the spread of the uninfected cytotype. This system is then expected to proceed to fixation of uninfecteds at which point the population will have gone full circle (reversible evolution). This evolutionary trajectory is supported by mitochondrial haplotype/Wolbachia cytotype covariance in Drosophila melanogaster. Given that there is no evidence of intra-specific horizontal transmission and that the most robust equilibrium is fixation of uninfecteds, a further consequence is that one can deduce that clade selection most likely favoured Wolbachia's ability to undergo inter-specific transmission. This possibility is supported by comparison of inter-species horizontal transmission rates of mutualistic and deleterious symbionts. Reversible evolution may well be a property of many (but not all) selfish genetic elements.

Original publication

DOI

10.1098/rspb.1996.0016

Type

Journal article

Journal

Proceedings of the Royal Society B: Biological Sciences

Publication Date

01/01/1996

Volume

263

Pages

97 - 104