Evolutionary dynamics of transposable elements in bdelloid rotifers

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

doi:10.7554/elife.63194

Cited by 33 publications

(37 citation statements)

References 181 publications

(282 reference statements)

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“…Empirically, several studies have attempted to address this question by comparing the TE load in natural sexual and related asexual lineages. For example, bdelloid rotifers, which have abandoned sexual reproduction millions of years ago ( Welch and Meselson 2000 ), are known to have lost all active retrotransposons ( Arkhipova and Meselson 2000 , but see Nowell et al 2021 ). However, there are also instances where sexual and related asexual lineages show no significant difference in TE prevalence ( Ågren et al.…”

Section: Introductionmentioning

confidence: 99%

Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Chen

Zhang

2021

Molecular Biology and Evolution

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Compared with asexual reproduction, sex facilitates the transmission of transposable elements (TEs) from one genome to another, but boosts the efficacy of selection against deleterious TEs. Thus, theoretically, it is unclear whether sex has a positive net effect on TE’s proliferation. An empirical study concluded that sex is at the root of TE’s evolutionary success because the yeast TE load was found to decrease rapidly in approximately 1000 generations of asexual but not sexual experimental evolution. However, this finding contradicts the maintenance of TEs in natural yeast populations where sexual reproduction occurs extremely infrequently. Here we show that the purported TE load reduction during asexual experimental evolution is likely an artifact of low genomic sequencing coverages. We observe stable TE loads in both sexual and asexual experimental evolution from multiple yeast datasets with sufficient coverages. To understand the evolutionary dynamics of yeast TEs, we turn to asexual mutation accumulation (MA) lines that have been under virtually no selection. We find that both TE transposition and excision rates per generation, but not their difference, tend to be higher in environments where yeast grows more slowly. However, the transposition rate is not significantly higher than the excision rate and the variance of the TE number among natural strains is close to its neutral expectation, suggesting that selection against TEs is at best weak in yeast. We conclude that the yeast TE load is maintained largely by a transposition-excision balance and that the influence of sex remains unclear.

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Section: Introductionmentioning

confidence: 99%

Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Chen

Zhang

2021

Molecular Biology and Evolution

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“…As TE mobilisation through a population is thought to be facilitated by sexual reproduction of their hosts, can TEs be strong drivers of genome evolution in asexual organisms? Interestingly, bdelloid rotifers are asexual animals that display features similar to those observed in R. irregularis : 1) recent and ongoing TE activity, 2) large expansions of RNAi pathway genes (~ 22 Argonaute, 4 Dicer and 37 RdRP) (66), and 3) targeting of TEs by small RNA (67). In this case, cryptic recombination was not found to support the inheritance of TE loci.…”

Section: Discussionmentioning

confidence: 95%

“…Without sex and recombination, organisms have limited ways of defending their genomes against unchecked TE expansions. As Nowell et al, propose (66), RNAi may have been required for ancient transitions from sexuality to asexuality. Thus, a controlled balance between TE activity and silencing may have enabled the long term ecological success of AM fungi.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional activity and epigenetic regulation of transposable elements in the symbiotic fungusRhizophagus irregularis

Dallaire

Manley

Wilkens³

et al. 2021

Preprint

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Arbuscular mycorrhizal (AM) fungi form mutualistic relationships with most land plant species. AM fungi have long been considered as ancient asexuals. Long-term clonal evolution would be remarkable for a eukaryotic lineage and suggests the importance of alternative mechanisms to promote genetic variability facilitating adaptation. Here, we assessed the potential of transposable elements (TEs) for generating genomic diversity. The dynamic expression of TEs during Rhizophagus irregularis spore development suggests ongoing TE activity. We find Mutator-like elements located near genes belonging to highly expanded gene families. Characterising the epigenomic status of R. irregularis provides evidence of DNA methylation and small RNA production occurring at TE loci. Our results support a potential role for TEs in shaping the genome, and roles for DNA methylation and small RNA-mediated silencing in regulating TEs. A well-controlled balance between TE activity and repression may therefore contribute to genome evolution in AM fungi.

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“…Thus, within Monogononta, larger genome size has been associated with the spread of transposable elements [ 22 ]. In Bdelloidea, genome duplication laid the basis for greater genomes although subsequent losses of genome parts obscure the original pattern of tetraploidy [ 20 , 21 , 65 – 67 ]. In line with this, we found the percentage of duplicated BUSCO Metazoa genes increased in the bdelloid A. vaga , whereas duplicated BUSCO genes were rare in the drafts for acanthocephalan, monogonont and seisonid genomes (Table 4 ).…”

Section: Discussionmentioning

confidence: 99%

Genomics and transcriptomics of epizoic Seisonidea (Rotifera, syn. Syndermata) reveal strain formation and gradual gene loss with growing ties to the host

et al. 2021

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Background Seisonidea (also Seisonacea or Seisonidae) is a group of small animals living on marine crustaceans (Nebalia spec.) with only four species described so far. Its monophyletic origin with mostly free-living wheel animals (Monogononta, Bdelloidea) and endoparasitic thorny-headed worms (Acanthocephala) is widely accepted. However, the phylogenetic relationships inside the Rotifera-Acanthocephala clade (Rotifera sensulato or Syndermata) are subject to ongoing debate, with consequences for our understanding of how genomes and lifestyles might have evolved. To gain new insights, we analyzed first drafts of the genome and transcriptome of the key taxon Seisonidea. Results Analyses of gDNA-Seq and mRNA-Seq data uncovered two genetically distinct lineages in Seison nebaliae Grube, 1861 off the French Channel coast. Their mitochondrial haplotypes shared only 82% sequence identity despite identical gene order. In the nuclear genome, distinct linages were reflected in different gene compactness, GC content and codon usage. The haploid nuclear genome spans ca. 46 Mb, of which 96% were reconstructed. According to ~ 23,000 SuperTranscripts, gene number in S. nebaliae should be within the range published for other members of Rotifera-Acanthocephala. Consistent with this, numbers of metazoan core orthologues and ANTP-type transcriptional regulatory genes in the S. nebaliae genome assembly were between the corresponding numbers in the other assemblies analyzed. We additionally provide evidence that a basal branching of Seisonidea within Rotifera-Acanthocephala could reflect attraction to the outgroup. Accordingly, rooting via a reconstructed ancestral sequence led to monophyletic Pararotatoria (Seisonidea+Acanthocephala) within Hemirotifera (Bdelloidea+Pararotatoria). Conclusion Matching genome/transcriptome metrics with the above phylogenetic hypothesis suggests that a haploid nuclear genome of about 50 Mb represents the plesiomorphic state for Rotifera-Acanthocephala. Smaller genome size in S. nebaliae probably results from subsequent reduction. In contrast, genome size should have increased independently in monogononts as well as bdelloid and acanthocephalan stem lines. The present data additionally indicate a decrease in gene repertoire from free-living to epizoic and endoparasitic lifestyles. Potentially, this reflects corresponding steps from the root of Rotifera-Acanthocephala via the last common ancestors of Hemirotifera and Pararotatoria to the one of Acanthocephala. Lastly, rooting via a reconstructed ancestral sequence may prove useful in phylogenetic analyses of other deep splits.

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Evolutionary dynamics of transposable elements in bdelloid rotifers

Cited by 33 publications

References 181 publications

Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Transcriptional activity and epigenetic regulation of transposable elements in the symbiotic fungusRhizophagus irregularis

Genomics and transcriptomics of epizoic Seisonidea (Rotifera, syn. Syndermata) reveal strain formation and gradual gene loss with growing ties to the host

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