Origin of sex for error repair. III. Selfish sex

Abstract

According to the repair hypothesis, sex originated as a cooperative interaction-the benefit being damage repair. As with all cooperative strategies, cooperative sex may be vulnerable to selfish mutants. The purpose of the present paper is to understand what implications such selfish mutants may have both for the origin of sex, especially in competition with asexual diploidy, and for the elaboration of the sexual cycle, especially in facultatively sexual organisms. Asexual diploids are assumed to effectively and instantaneously repair all damages without expression of deleterious recessive mutations. Costs to asexual diploidy are considered in terms of its birth rate and mortality rate. The main results of the present paper are as follows. (i) Asexual diploidy wins when the costs of diploidy are small, mortality rates low, and damage rates high. (ii) Beginning with an ancestral state in which cells are asexual haploids, the sexual life cycle would emerge before asexual diploidy as a response to increasing DNA damage. (iii) Selfish sex is a far more robust repair strategy than cooperative sex, especially in competition with asexual diploidy. (iv) Although cooperative sex is more adaptive in extreme environments characterized by high damage and high mortality, selfish sex can still invade in these regions and take the entire system to extinction. (v) Once it is present, selfish sex is stable to asexual diploidy over a wide range of parameter values and can persist in regions of parameter space forbidded to the asexual diploid. These results help to address a concern of the gene repair theory of sex, which is that efficient repair in an asexual diploid is a better strategy than sex. Data from microbes bearing on the results are discussed as is the relationship between facultative sex in multicellular organisms and selfish sex in microbes.