Evolutionary dynamics of transposable elements in bdelloid rotifers

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 where males are thus far unknown. Contrary to expectations, we find a diverse range 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, but we report that bdelloids share a large and unusual expansion of genes involved in RNAi-mediated TE suppression. This suggests that enhanced cellular defence mechanisms might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.

Evolutionary dynamics of transposable elements in bdelloid rotifers

“…We first compared the bdelloid genomes to the other available syndermatan genomes. The sampled monogonont genomes are slightly more TE-rich than the bdelloids with a mean of 5.2% ± 1.5 SD class I TEs and 2.5% ± 1.0 SD class II TEs ( Figure 2A , Figure 2—figure supplements 1 and 2 , Figure 2—source data 1 , Nowell et al, 2021 ). Repeat content differs on average from the bdelloids mainly in the composition of two types of class I retrotransposons.…”

“…To ascertain the repeat content of bdelloid genomes relative to other taxa in a consistent manner, we used the RepeatModeler and RepeatMasker pipelines to identify and classify repeats across all of the sampled genomes. The total proportion of the genome classified as repetitive ranged from ~19% to 45% across bdelloid genera, with variation within and between species ( Figure 2A , Figure 2—figure supplements 1 and 2 , Figure 2—source data 1 , Nowell et al, 2021 ). Most of these are simple or unclassified repeats that do not belong to major TE superfamilies.…”

“…TE lengths of individual TEs were parsed directly from the final TE annotation ( Nowell et al, 2021 ). Since this resulted in >1 million observations, TE lengths were averaged to the superfamily level using the classification system of Kapitonov and Jurka, 2008 to assign superfamilies (i.e.…”

An ancient clade ofPenelope-like retroelements with permuted domains is present in the green lineage and protists, and dominates many invertebrate genomes

“…While cataloguing PLEs in several recently sequenced genomes, such as the acanthocephalan (Pomphorhynchus laevis) and a bdelloid rotifer (Didymodactylos carnosus), as well as a darwinulid ostracod (Darwinula stevensoni) (Mauer, et al 2020;Nowell, et al 2021;Schön, et al 2021), we noticed the absence of the GIY-YIG domain at the C-terminus of several PLEs, which is typically indicative of EN-PLEs. In these cases, however, extending the 5'-end of the frequently truncated PLE copies revealed a conserved N-terminal GIY-YIG EN domain, typically 220-275 aa in length.…”