Genome reduction as the dominant mode of evolution

Abstract

A common belief is that evolution generally proceeds towards greater complexity at both the organismal and the genomic level, numerous examples of reductive evolution of parasites and symbionts notwithstanding. However, recent evolutionary reconstructions challenge this notion. Two notable examples are the reconstruction of the complex archaeal ancestor and the intron-rich ancestor of eukaryotes. In both cases, evolution in most of the lineages was apparently dominated by extensive loss of genes and introns, respectively. These and many other cases of reductive evolution are consistent with a general model composed of two distinct evolutionary phases: the short, explosive, innovation phase that leads to an abrupt increase in genome complexity, followed by a much longer reductive phase, which encompasses either a neutral ratchet of genetic material loss or adaptive genome streamlining. Quantitatively, the evolution of genomes appears to be dominated by reduction and simplification, punctuated by episodes of complexification.

Theory of prokaryotic genome evolution

“…Thus, it seems likely that, most of the time, the majority of the genomes are somewhat smaller than the long-term equilibrium size. A biologically plausible scenario is that prokaryotes are exposed to beneficial genetic material only for short periods of time, resulting in brief intervals of fast growth followed by slow genome shrinking (30). Steady state is possible under this scenario as well but only as the average over multiple cycles of gain and loss, which probably occur on a timescale much longer than the scale of the ATGC evolution.…”

Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean

“…The genome streamlining hypothesis argues that species with large effective population sizes are under selective pressures that favor small genomes, reducing the material or energetic cost of cellular replication in nutrient-poor environments (47,48). Streamlined genomes are found in diverse, uncultivated bacteria in the oligotrophic ocean (49,50), and it has been suggested that evolution of the Archaea, in particular, has been dominated by reductive selection (51). As exemplified by Prochlorococcus (52), the uncultivated bacterial clade SAR86 (50), and Pelagibacter (39), reductive selection can result in a loss of metabolic versatility or nutritional dependencies (53), such as the loss of pathways for assimilation of oxidized forms of nitrogen or essential vitamin cofactors.…”

Beyond the Black Queen Hypothesis

“…Although evolution is usually associated with genome complexification (Wolf and Koonin, 2013), in the BQH the source of evolutionary opportunities is simplification through gene loss. Typically, gene loss results from two different forces: genetic drift and positive selection.…”