Dynamics of transposable elements: towards a community ecology of the genome

Abstract

Like ecological communities, which vary in species composition, eukaryote genomes differ in the amount and diversity of transposable elements (TEs) that they harbor. Because TEs have a considerable impact on the biology of their host species, we need to better understand whether their dynamics reflects some form of organization or is primarily driven by stochastic processes. Here we borrow ecological concepts on species diversity to explore how interactions between TEs can contribute to structure TE communities within their genomic ecosystem. Whereas the niche theory predicts a stable diversity of TEs because of their divergent characteristics, the neutral theory of biodiversity predicts the assembly of TE communities from stochastic processes acting at the level of individual TE. Contrary to ecological communities, however, TE communities are shaped by selection at the level of their ecosystem, i.e., the host individual. Developing ecological models specific to the genome will thus be pre-requisite for modeling the dynamics of TEs. Towards an ecology of the genomeTransposable elements (TEs) constitute a large proportion of many multicellular eukaryote genomes, from 4% in the yeast Saccharomyces cerevisiae to more than 70 % in some plants and amphibians, and 45% in human [1]. The mobility and amplification of TEs represent a major source of genomic variation either by virtue of their insertion or by triggering a variety of small-and large-scale chromosomal rearrangements. Once inserted, most TE copies serve no immediate function and thus their sequences progressively decay by accumulating mutations at the neutral rate of the species and eventually disappear. Occasionally, some TE copies may be co-opted by the genome to function either as coding sequences or as regulatory elements [2]. Whereas TEs can be said to contribute genetic variation and therefore innovation [1][2][3][4][5][6], their uncontrolled movement and proliferation pose a threat to genome integrity. Indeed, TEs are an important cause of deleterious mutations and illnesses, including in humans [7][8], and therefore several host-encoded mechanisms exist to silence or restrict their activity [9][10][11][12].TEs are classified into different classes and subclasses on the basis of their structural organization and of mechanisms of transposition (DNA transposons, Long Terminal Repeat (LTR) retrotransposons, non-LTR retrotransposons…) [1], and further divided into families and sub-families (see Box 1). Genomes of different organisms contain widely differing numbers of TE families and of TE copy numbers per family (Box 1). The main challenge we are facing is therefore to understand to what extent the contrasted patterns and variations that Corresponding author: Venner, we see across genomes in the amount and diversity of TEs reflect some sort of organization, or whether they are largely idiosyncratic, i.e., the result of stochastic processes. The dynamics of TEs has been modeled on the basis of their transposition and excision rates and their fitne...

Experimental evolution reveals hyperparasitic interactions among transposable elements

“…It has been recently suggested that the relationships between genome components (including genes, transposable elements, or any sequence able to persist over evolutionary time) were similar to the relationships between individuals or species in ecosystems (10,49,50), although the possibility to apply ecological formalism to genome evolution remains questionable (51). Here, we brought substantial evidence that the relationships between autonomous and nonautonomous mariner TE copies were analogous to parasitism: Mos1 copies (the "hosts") are able to survive and replicate by themselves, whereas peach copies (the "parasites") are unable to transpose without Mos1 copies.…”

A Brief History of the Status of Transposable Elements: From Junk DNA to Major Players in Evolution

“…TEs must therefore be considered to be integrated components of the genomes, which have played a major role in evolution. It is proposed that it might be more accurate to view the genome as an ecological ecosystem in which the TE families and subfamilies correspond to the ''species'' of an ecosystem (Brookfield 2005;Mauricio 2005;Le Rouzic et al 2007;Venner et al 2009). These ideas suggest that the term ''controlling element,'' initially proposed by B. McClintock, was appropriate, even if all TE insertions do not have this ''gene-controlling'' capacity.…”

Env-less endogenous retroviruses are genomic superspreaders

“…For example, workers have attempted to explain the proliferation of individual TE lineages and why the genomes of more complex organisms tend to contain more TEs than do simpler ones (11,12). We take an approach common in community ecology and ask what controls the relative abundance of different TE lineages.…”