Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Abstract

Sexual reproduction is a trait shared by all complex life, but explaining its origin and evolution remains a major theoretical challenge. Virtually all theoretical work on the evolution of sex has focused on the benefits of reciprocal recombination among nuclear genes, paying little attention to the dynamics of mitochondrial genes. Here I develop a mathematical model to study the evolution of alleles inducing cell fusion in an ancestral population of clonal proto-eukaryotes. Mitochondrial mixing masks the detrimental effects of faulty organelles and drives the evolution of sexual cell fusion despite the declining long-term population fitness. Cell-fusion alleles fix under negative epistatic interactions between mitochondrial mutations and strong purifying selection, low mutation load and weak mitochondrial-nuclear associations. I argue that similar conditions could have been maintained throughout the eukaryogenesis, favoring the evolution of sexual cell fusion and meiotic recombination without compromising the stability of the emerging complex cell.