Neutral Theory, Transposable Elements, and Eukaryotic Genome Evolution

Abstract

Among the multitude of papers published yearly in scientific journals, precious few publications may be worth looking back in half a century to appreciate the significance of the discoveries that would later become common knowledge and get a chance to shape a field or several adjacent fields. Here, Kimura's fundamental concept of neutral mutation-random drift, which was published 50 years ago, is re-examined in light of its pervasive influence on comparative genomics and, more specifically, on the contribution of transposable elements to eukaryotic genome evolution.

Fig. 1.

Transposable element dynamics and insertion patterns in eukaryotic genomes. (A) Examples of differing modes of intragenomic TE proliferation and maintenance over time (t), influenced by the strength of host response. Green, “benign” TEs adapted to intragenomic “safe havens” with copy numbers at equilibrium. Red, “aggressive” TEs which periodically invade, amplify, get suppressed, and undergo slow decay (e.g. by point mutation). Blue, “dormant” TEs subject to waves of amplification, suppression, and faster decay (e.g. by hypermutation or deletion). If amplification and decay rates are equal, there is no skew. TE content is typically measured in percentage of the genome (Y axis). (B) Major types of eukaryotic genome organization on a 100% scale, regardless of actual size. CDS, % genome covered by coding sequences (including introns); R, regulatory regions; TE, transposable element sequences; S, high-copy repeats and satellites; ?, sequences of unknown origin. New TE insertions are shown by arrows; crossed arrows, subject to negative selection; thicker arrows, insertions with adaptive potential. Double-headed arrows denote the possibility of TE conversion into regulatory regions or decay beyond recognition; curly bracket, the possibility of noncoding DNA removal from oversized germline genomes (as in ciliates). Streamlined genomes (as in yeast) have few TEs, which are mostly confined to preferred targets. In oversized genomes, TEs occupy most of the genome, and their turnover rate may be either low (as in mammals) or high (as in most plants). All generalizations are for illustrative purposes only; individual genomes and TE types may combine different features.