The Maintenance of Sex: Ronald Fisher meets the Red Queen

The Maintenance of Sex: Ronald Fisher meets the Red Queen
David Green, Chris Mason
(Submitted on 10 Apr 2013)

Sex in higher diploids carries a two-fold cost of males that should reduce its fitness relative to cloning and result in extinction. Instead, sex is widespread and it is clonal species that face early obsolescence. One possible reason is that sex is an adaptation to resist parasites. We use computer simulations of finite populations to model a Red Queen in which a parasitic haploid mounts a negative frequency-dependent attack on a diploid host. Both host and parasite populations generate novel alleles by mutation and have access to large allele spaces. Sex outcompetes cloning by two overlapping mechanisms. First, sexual diploids adopt advantageous homozygous mutations more rapidly than clonal diploids under conditions of lag load. This rate advantage can offset the lesser fecundity of sex. Second, a relative advantage to sex emerges under host mutation rates that are fast enough to retain fitness in a rapidly mutating parasite environment and increase host polymorphism and polyclonality. Polyclonal populations disproportionately experience interference with selection at high mutation rates, both between and within loci, slowing clonal population adaptation to a changing parasite environment and reducing clonal population fitness relative to sex. This effect increases markedly with the number of loci under independent selection. Rates of parasite mutation exist that not only allow sex to survive despite the two-fold cost of males but which enable sexual and clonal populations to have equal fitness and co-exist. Since all higher organisms carry parasitic loads, the model is of general applicability.

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