Horizontal gene transfer as a possible evolutionary predecessor of sexual reproduction

Abstract

Computer modeling shows that high rates of lateral gene transfer (LGT), combined with homologous recombination, enhance selection efficiency, thus making it possible for organisms to acquire larger genomes without irreversible growth of mutation load. In prokaryotes, the optimal (high) rate of LGT cannot evolve because of the “suicidal effect” of modifiers, i.e., alleles that enhance LGT are systematically replaced by alleles that hinder LGT and never vice versa. Therefore, the latter alleles spread despite the fact that they reduce fitness of organisms and populations. This “conflict of interests” can be resolved via evolution of whole-genome reciprocal recombination, which effectively removes the basis for propagation of “selfish” modifiers. Eukaryotic sexual reproduction (amphimixis) probably appeared as the final result of evolution of mechanisms of LGT driven by selection for high interindividual recombination rate. Such selection could have been facilitated at the early stages of eukaryogenesis due to an increase in genome size and high mutation rate caused by higher O2 concentration and invasion of group II introns.