Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Abstract

Prokaryotes generally reproduce clonally but can also acquire new genetic material via lateral gene transfer (LGT). Like sex, LGT can prevent the accumulation of deleterious mutations predicted by Mullers ratchet for asexual populations. This similarity between sex and LGT raises the question why did eukaryotes abandon LGT in favor of sexual reproduction? Understanding the limitations of LGT provides insight into this evolutionary transition. We model the evolution of a haploid population undergoing LGT at a rate{lambda} and subjected to a mutation rate . We take into account recombination length, L, and genome size, g, neglected by previous theoretical models. We confirm that LGT counters Mullers ratchet by reducing the rate of fixation of deleterious mutations in small genomes. We then demonstrate that this beneficial effect declines rapidly with genome size. Populations with larger genomes are subjected to a faster rate of fixation of deleterious mutations and become more vulnerable to stochastic frequency fluctuations. Mullers ratchet therefore generates a strong constraint on genome size. Importantly, we show that the degeneration of larger genomes can be resisted by increases in the recombination length, the average number of contiguous genes drawn from the environment for LGT. Large increases in genome size, as in early eukaryotes, are only possible as L reaches the same order of magnitude as g. This requirement for recombination across the whole genome can explain the strong selective pressure towards the evolution of sexual cell fusion and reciprocal recombination during early eukaryotic evolution - the origin of meiotic sex.