Abstract

BackgroundThe nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). To date, the precise evolutionary and ecological conditions influencing TE accumulation remain poorly understood. Most previous attempts to identify these conditions have focused on evolutionary processes occurring at the host organism level, whereas we explore a TE ecology explanation.ResultsAs an alternative (or additional) hypothesis, we propose that ecological mechanisms occurring within the host cell may contribute to patterns of TE accumulation. To test this idea, we conducted a series of experiments using a simulated asexual TE/host system. Each experiment tracked the accumulation rate for a given type of TE within a particular host genome. TEs in this system had a net deleterious effect on host fitness, which did not change over the course of experiments. As one might expect, in the majority of experiments TEs were either purged from the genome or drove the host population to extinction. However, in an intriguing handful of cases, TEs co-existed with hosts and accumulated to very large numbers. This tended to occur when TEs achieved a stable density relative to non-TE sequences in the genome (as opposed to reaching any particular absolute number). In our model, the only way to maintain a stable density was for TEs to generate new, inactive copies at a rate that balanced with the production of active (replicating) copies.ConclusionsFrom a TE ecology perspective, we suggest this could be interpreted as a case of ecosystem engineering within the genome, where TEs persist by creating their own “habitat”.

Highlights

  • The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs)

  • We propose that the TE ecosystem engineering hypothesis identifies a distinct process that potentially contributes to variability in genome size among species

  • We do not take ourselves to have provided evidence that, in nature, the capacity for TEs to accumulate and remain active in most eukaryotic genomes is due to TE ecosystem engineering

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Summary

Introduction

The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). Transposable elements (TEs) make up a large fraction of all but the most diminutive eukaryotic genomes and are the most prominent contributors to the enormous variability in nuclear genome size [1] They make up a small but significant portion of many prokaryotic genomes [2, 3]. 40 years ago, the classic “selfish DNA” papers sought to characterize sequences such as TEs as biological entities with properties that could promote their accumulation even at the expense of host fitness [9, 10] These early papers noted that, on occasion, initially selfish DNA elements could be co-opted into functional roles at the organism level. It is important to note that the categories, below, apply to individual TE families (or even individual copies or lineages within a family) and not to genomes as a whole; a given genome may be home to diverse TEs that occupy any number of these categories

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