Evolutionary dynamics of transposable elements in bdelloid rotifers.

Reuben W Nowell,Timothy G Barraclough,Christopher G Wilson,Fernando Rodriguez,Pedro Almeida,Diego Fontaneto,Lutz Becks,Irina R Arkhipova,Philipp H Schiffer

doi:10.7554/elife.63194

Abstract

Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates in which males are thus far unknown. Contrary to expectations, we find a variety of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms. Instead, we find that that TE content evolves relatively slowly in bdelloids and that gene families involved in RNAi-mediated TE suppression have undergone significant expansion, which might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.

Highlights

Transposable elements (TEs) are repeated sequences of DNA that can mobilize and replicate themselves within genomes (Charlesworth and Charlesworth, 1983; Hickey, 1982; Orgel and Crick, 1980)
‘Silwood-1’) and BUSCO scores 207 that indicated 89–98% of 303 core eukaryote genes were completely recovered, increasing to 96– 208 99% if fragmented BUSCO copies are included (Table 1). General genome characteristics such as genome size, the proportion of G + C nucleotides (GC%), the number of coding genes (CDS), and the level of homologous divergence were within the range expected from previous analyses of bdelloid genomes (Flot et al, 2013; Nowell et al, 2018) (Figure 1B–C, Table 1, Figure 1—figure supplement 1). Intragenomic collinearity and synonymous divergence of coding regions in the A. steineri, R. sordida and R. sp
At the taxonomic level of class and above, the model detects a significant increase in Argonaute copies in the branch leading to the nematode C. elegans, driven by the well-known ‘worm-specific’ Ago (WAGO) genes found in nematodes (Buck and Blaxter, 2013; Shi et al, 2013; Yigit et al, 2006)

Summary

Introduction

Transposable elements (TEs) are repeated sequences of DNA that can mobilize and replicate themselves within genomes (Charlesworth and Charlesworth, 1983; Hickey, 1982; Orgel and Crick, 1980). 84 Models of the population genetics of vertically transmitted TEs in asexuals predict one of two outcomes: either TEs accumulate within lineages faster than they can be removed, overrunning each lineage in turn and driving the population extinct, or, TE removal outweighs proliferation and the population eventually purges itself entirely of deleterious TEs (Boutin et al, 2012; Dolgin and Charlesworth, 2006; Startek et al, 2013) These predictions should apply to TEs from the LINE-like group of class I retroelements, as these are thought to be almost exclusively vertically transmitted owing to the instability of the extrachromosomal RNA intermediate (Eickbush and Malik, 2002; Peccoud et al, 2017; Robertson, 2002; Schaack et al, 2010b; Silva et al, 2004). These predictions are difficult to test empirically, because it is expected to take millions of generations for an asexual population to either eliminate TEs or go extinct (Dolgin and Charlesworth, 2006), too long to observe directly and beyond the lifespan of most asexual lineages (Jaron et al, 2020; Neiman et al., 2009)

Methods

Results

Conclusion