Fundamental asymmetry of insertions and deletions in genomes size evolution

Abstract

The origin of large genomes that underlies the long standing “C-value enigma” is only partially explained by selfish DNA. We investigated insertions and deletions (indels) of nucleotides and discussed their relevance in size evolution of random biological sequences (RBS) and genomes. By developing a probabilistic model of RBS based on size evolution of expandable sites in a thought perfect genome, it was found that insertion bias engenders exponential increase of average RBS sizes. When combined with existing large segments of genome that are not subject to selection pressure (e.g. selfish DNA), such insertion bias results in explosive expansion of genomes, and therefore helps explain the “C value enigma” besides selfish DNA. Such increase of RBS size is caused by the fundamental asymmetry of indels, with insertions result in more available sites and deletions result in less deletable nucleotides. In qualitative agreement with the size distribution of known genomes, tails of RBS size distributions exhibit exponential decay with probabilities of larger RBS segments being smaller. Unsurprisingly, a slight deletion bias (higher deletions probabilities) results in a slow decrease of average RBS size and may lead to their eventual vanishing. Contrary to intuition, strictly balanced insertion and deletion results in linearly increasing instead of completely fixed RBS size. Nonetheless, such slow linear increase of average RBS sizes with time are small in magnitude and are consequently not influential on genome size evolution, and certainly not a major contributor for the “C-value enigma”. Our model suggested that insertion bias of nucleotides may provide complementary explanation for large genomes besides selfish DNA. The fundamental indel asymmetry is applicable for all forms of genomic insertions and deletions. Long-lasting exponential increase of genome size present energy and material requirement that is impossible to sustain. We therefore concluded that if there were explosively accelerating expansion caused by significant effective insertion bias for any survival species, it must have occurred sporadically. Our model also provided an explanation for the observed proportional evolution of genome size.