Evolution of linkage and genome expansion in protocells: The origin of chromosomes

Abstract

Chromosomes are likely to have assembled from unlinked genes in early evolution. Genetic linkage reduces the assortment load and intragenomic conflict in reproducing protocell models to the extent that chromosomes can go to fixation even if chromosomes suffer from a replicative disadvantage, relative to unlinked genes, proportional to their length. Here we numerically show that chromosomes spread within protocells even if recurrent deleterious mutations affecting replicating genes (as ribozymes) are considered. Dosage effect selects for optimal genomic composition within protocells that carries over to the genic composition of emerging chromosomes. Lacking an accurate segregation mechanism, protocells continue to benefit from the stochastic corrector principle (group selection of early replicators), but now at the chromosome level. A remarkable feature of this process is the appearance of multigene families (in optimal genic proportions) on chromosomes. An added benefit of chromosome formation is an increase in the selectively maintainable genome size (number of different genes), primarily due to the marked reduction of the assortment load. The establishment of chromosomes is under strong positive selection in protocells harboring unlinked genes. The error threshold of replication is raised to higher genome size by linkage due to the fact that deleterious mutations affecting protocells metabolism (hence fitness) show antagonistic (diminishing return) epistasis. This result strengthens the established benefit conferred by chromosomes on protocells allowing for the fixation of highly specific and efficient enzymes.

Author summary

The emergence of chromosomes harboring several genes is a crucial ingredient of the major evolutionary transition from naked replicators to cells. Linkage of replicating genes reduces conflict between them and alleviates the problem of chance loss of genes upon stochastic protocell fission. The emerging organization of protocells maintaining several segregating chromosomes with balanced gene composition also allows for an increase in the number of gene types despite recurrent deleterious mutations. We suggest that this interim genomic organization enabled protocells to evolve specific and efficient enzymes and paved the way toward an accurate mechanism for chromosome segregation later in evolution.