The origin of meiotic sex is a long-standing evolutionary enigma. This novel mechanism of reproduction replaced lateral gene transfer (LGT), the uptake and recombination of pieces of environmental DNA seen in bacteria and archaea. We link its origin to the expanded genome size and proliferation of genetic repeats found in early eukaryotes. Both factors led to high levels of mutation accumulation and gene loss under LGT, which could not be retarded through increases in the rate of LGT or the length of DNA recombined. Meiotic sex with homologous pairing of long-chromosome-sized pieces of DNA promoted purifying selection and suppressed ectopic recombination. It permitted the evolution of the expanded genome needed for the evolution of complex eukaryotic life.
The transition from prokaryotic lateral gene transfer to eukaryotic meiotic sex is poorly understood. Phylogenetic evidence suggests that it was tightly linked to eukaryogenesis, which involved an unprecedented rise in both genome size and the density of genetic repeats. Expansion of genome size raised the severity of Muller’s ratchet, while limiting the effectiveness of lateral gene transfer (LGT) at purging deleterious mutations. In principle, an increase in recombination length combined with higher rates of LGT could solve this problem. Here, we show using a computational model that this solution fails in the presence of genetic repeats prevalent in early eukaryotes. The model demon- strates that dispersed repeat sequences allow ectopic recombination, which leads to the loss of genetic information and curtails the capacity of LGT to prevent mutation accu- mulation. Increasing recombination length in the presence of repeat sequences exacer- bates the problem. Mutational decay can only be resisted with homology along extended sequences of DNA. We conclude that the transition to homologous pairing along linear chromosomes was a key innovation in meiotic sex, which was instrumental in the expansion of eukaryotic genomes and morphological complexity.