Evolutionary dynamics of transposable elements in bdelloid rotifers

  1. Reuben W Nowell
  2. Christopher G Wilson
  3. Pedro Almeida
  4. Philipp H Schiffer
  5. Diego Fontaneto
  6. Lutz Becks
  7. Fernando Rodriguez
  8. Irina R Arkhipova
  9. Timothy G Barraclough

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    Summary: Nowell et. al. present an analysis of transposable elements (TEs) in bdelloid rotifers and compare their dynamics to those in related species. Through this comparative analysis, the authors test various evolutionary hypotheses about asexual genomes, as well as recent suggestions that these ancient asexual organisms may not actually be asexual. Nowell et. al. find no evidence supporting the presence of recombination (and thus, sex) in bdelloid rotifers, and no strong predicted evolutionary signatures of asexuality in TE dynamics in these species. Additionally, they find evidence for expansion of RNAi-related genes, which may play a role in countering the expected TE dynamics in asexual species. Overall, this work is substantial, thorough, and presents some answers to long-standing questions about the genome evolution of long-term asexual species.

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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.

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  1. Version published to 10.7554/elife.63194 on eLife
  2. eLife

    Reviewer #3:

    Substantive concerns:

    1. Regarding hypothesis 4, the authors test whether or not desiccating species have lower TE loads than non-desiccating species, but in my opinion the logic outlined in lines 114-124 suggests that the relationship between desiccation and TE load may be more nuanced than overall TE load. It could be possible that DSB repair associated with desiccation removes only recent insertions if homologous pairing is involved, or high-copy TEs if ectopic recombination has occurred. The authors already test recent TE activity elsewhere in the manuscript, so they could compare signatures of recent activity in desiccating vs non-desiccating species to see if there are fewer recently active TEs in desiccation species. Similar comparisons could easily be made for abundance of high-copy TEs (regardless of length).

    2. Additionally, regarding the signatures of recent transposition, the authors have done a thorough job comparing TE divergences and LTR insertions, but since transcriptomes for some species are available, presence of transcribed TEs could provide further support for recent and ongoing TE activity.

  3. eLife

    Reviewer #2:

    This manuscript represents a very considerable amount of work, both wet lab and analytic, constituting excellent science. This may be the best paper yet produced on Bdelloids. Despite this glowing recommendation I have some very significant concerns about certain parts, their conclusions section, and the evidence for "enhanced cellular defence mechanisms" in the abstract. Some parts are very rigorous, but others give in to excess speculation. This paper does not really need additional work, it needs some re-writing. Afterwards this important manuscript would be a welcome addition to the field, even without the supposedly unique defence mechanisms.

    Substantive concerns:

    1. Line 273 onwards: There is a comparison in the manuscript between Bdelloids and Monogonants. It wasn't clear to me however that these groups had been sampled sufficiently. The Monogonants are represented by 5 species (8 genomes) within a single genus in no way representing the diversity of Monogonants and the sampling of Bdelloids is also small. The authors should take a more cautious tone to any conclusions.

    2. Line 276-278: The rationale for focussing on this specific group of TEs did not appear robust. The authors say "this class of TEs is thought to be least likely to undergo horizontal transfer and thus the most dependent on sex for transmission". But other groups are not evolving predominantly by horizontal transfer, transposons can change without meiotic sex and this section needs writing a little more clearly. The following lines make a case that some transposon groups increase, and some decrease in frequency. The obvious hypothesis is drift, but the writing was unclear, I always felt that some other mechanism was being proposed but never really stated clearly.

    3. Lines 288-300, comparison of TE abundances across animals; this section was very poorly done. I thought the authors could delete this comparison and have a better manuscript. How were these other species chosen? Is C. elegans a good representative of the entire phylum Nematoda? Are the tardigrades representatives of their phylum? Assembly and annotation methods vary enormously across datasets so what can the authors conclude without standardising assembly and annotation for these other animal groups? The authors say "as expected, both the abundance and diversity of TEs varied widely across taxa" This was indeed expected, Figure 2b seems to show noise, and suggests to me that the inclusion of this data was not a good idea. I suggest it is removed, or a very substantive analysis and discussion of the way in which it is an accurate and representative sample of animal transposon loads is written.

    4. Line 350-353: This section is weak and needs to be improved. The authors need to make it very clear that this is not a test, it is a single observation. The phrase "as predicted by theory for elements dependent on vertical transmission" seems rather unsupported. Does this relate to the argument put forward in lines 276-278? It was unconvincing at this point also. The current description that some families increase and some decrease is couched in what sounds like too meaningful sounding language, which could be improved to be more consistent with the results. Lines 353-355 here seem to make an argument that the variation of TEs in bdelloids is purely a phylogenetic effect variably present in some bdelloid lineages and related groups. If this is their view (and it seems very reasonable indeed) then the manuscript would be improved considerably if they stated it more clearly.

    5. Lines 533-535 "consistent with a high fit of the data to the phylogeny under a Brownian motion model as would be expected if TE load evolves neutrally along branches of the phylogeny." I felt that this was a truly excellent result that needed to be put forward more strongly in other areas of the manuscript. In this area, and some others in this manuscript the authors have truly unique data dramatically improving our understanding of bdelloids. The manuscript would be improved if authors concentrated much less throughout on ideas this data is exceptional and different from other animals, and instead followed their own analysis that this fits with current biological thought.

    6. Lines 621-632: "no significant difference between monogononts and bdelloids, or between desiccating and non-desiccating bdelloids" It is not clear to me here what statistical test is being carried out. All tests require phylogenetic control of course. I do agree that they are quite similar, perhaps this should be rewritten to reflect only that?

    7. 705-706 The authors look at 3 gene families concerned with transposon control to examine copy number. In one of them they say "the RdRP domain in particular is significantly expanded". I am unclear of what test of significance was carried out and where to find this analysis. Unlike the query concerning desiccating and non-desiccating above I think this analysis is essential. The authors make a really big thing about the expansion of this gene family, including it in the abstract. If they wish to keep its prominence then they need to clearly show whether there is evidence that the size of this domain family is significantly expanded along the branch leading to bdelloids. I understand that this is illustrated in Figure 7 but this is not a test. This needs to be made much clearer in a quantitative rather than descriptive way. There is a need for broad taxonomic sampling, standardisation of assembly and annotation, and a phylogenetic design for this analysis. Else it should be removed or at the least described more conservatively.

    8. Line 725: "Why do bdelloids possess such a marked expansion of gene silencing machinery?" There is no evidence presented that they do. There may be a hypothesis that they do it differently, rather than more, but that also needs testing. There is a lot of speculation in this paragraph, and I think removing this whole paragraph would improve the manuscript.

    9. If there is an expansion of this family what can we then conclude? The authors say in the abstract "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" yet they also review that animal groups can utilize different gene families for transposon control. Is there evidence that clade 5 nematodes with PIWI have a quantitatively different transposon defence mechanism? No, they just use a different pathway to some other groups, and the default position surely has to be the same for bdelloids, there is no evidence presented that their defence is enhanced. I would strongly recommend that the authors reduce the strength of their claims about the significance of bdelloid transposon control gene families in this manuscript.

    10. I felt that the Conclusions (and Abstract) were too speculative and not fully supported by the existing data, though this can easily be addressed by a substantial re-write.

  4. eLife

    Reviewer #1:

    This manuscript investigates TE diversity and variation across several clades of bdelloid rotifers, which are particularly interesting from an evolutionary perspective since they reproduce asexually. As stated by the authors, theory predicts that asexuality may lead to two opposite outcomes in terms of TEs content. In the absence of sex, TEs may not easily jump into new genomic backgrounds where they are not repressed, leading to a decline in TE content. On the other hand, there is no recombination without sex, which removes the selective pressure against TEs due to their involvement in ectopic recombination. The authors show that despite these extreme expectations, asexual rotifers do not seem to display any of these patterns, although recent insertions seem rare and possibly brought through horizontal transfers. They do not observe any clear effect of adaptation to desiccation on TEs content, which seems to exclude any effect of enhanced DNA repair mechanisms in controlling TEs. They observe less LINEs and more (recent) DNA transposons in bdelloid rotifers, which is consistent with the absence of sex (limiting LINEs spread) and horizontal transfers (more frequent for DNA transposons). The expansion of RNAi gene silencing pathways suggests that asexuality comes at a cost, such as the proliferation of TEs, the accumulation of genetic load, and the control of horizontal gene transfers that might be deleterious. I think this supports the hypothesis of strong TEs activity associated with the onset of asexuality, leading to a strong evolutionary response. This suggests that these clades survived the arms race with TEs. This work shows how intricate the coevolutionary dynamics between TEs and their hosts can be. The manuscript is well-written, analyses are sound and detailed. I have a few general comments/questions that I detail below: Horizontal gene transfer: given the abundance of recent DNA transposons in some clades (class I), it may be worth discussing a bit more this possibility (at this stage it is mostly discussed in the Conclusion).

    If my understanding is correct, there is no assessment of TEs or SNPs heterozygosity for each individual. This might be interesting to explore. If TEs are deleterious recessive, one might observe more frequently at the heterozygous state. For intraspecific data, it may be interesting to look at how nucleotide diversity varies along the genome. Since variable recombination may be associated with diversity due to the effects of selection at linked sites, checking diversity along the genome may bring another layer of information about the frequency of sexual reproduction and its effects on TEs diversity. I acknowledge that this would be a rather exploratory analysis, and am not asking the authors to carry it, but I am curious to know how do methods designed to estimate effective recombination rates perform on these data (e.g. LDHat, or more recently iSMC for a single diploid genome).

    Question related to demography and selection: would it be possible to obtain estimates of the effective population size for these clades? It would be interesting to have such an estimate to get an idea of the efficiency of purifying selection against TEs, and whether Muller's ratchet could explain the current abundance of TEs (in the case of moderate/small effective population sizes). I liked the idea of using the ABC to test for consistency with asexuality, but am wondering to what extent it is biased by non-constant transposition rates, which cannot be properly modeled by the coalescent simulation? I would also assume these simulations do not take into account past changes in demography (I believe this option has not been included in the software yet). This is not necessarily a major issue for me, as long as these limitations are mentioned. When presenting the ABC framework in the Methods section, you may want to give more details about the part carried with the abc package itself (e.g. which regression/rejection algorithms were used, etc.).

    A few other comments linked to specific paragraphs/sentences:

    • L419: why choosing LTR-Rs in particular (abundance and the fact they are not class I I guess).
    • L450: Would it be possible to obtain a time in generations from, e.g., an approximate mutation rate?
    • L455: Would it be possible to call heterozygote SNPs/elements?
    • L550-656: do you examine the most recent elements only? It may be interesting to check these correlations for elements of different ages, since selection may have had the time to act on the most ancient TEs.
    • L642: It might also be that longer elements display functional regulatory/promoter regions, and have a stronger impact on fitness.
    • L725: I liked this part, but wondered if a slightly more detailed discussion was possible. As the authors state, the expansion of RNAi pathways is consistent with a control mechanism against TEs. It is important to detail alternative explanations since there is no functional evidence in this model that this expansion actually controls TEs proliferation (unless I missed something). Given the rather unique properties of these organisms, it may be worth discussing.
  5. eLife

    Summary: Nowell et. al. present an analysis of transposable elements (TEs) in bdelloid rotifers and compare their dynamics to those in related species. Through this comparative analysis, the authors test various evolutionary hypotheses about asexual genomes, as well as recent suggestions that these ancient asexual organisms may not actually be asexual. Nowell et. al. find no evidence supporting the presence of recombination (and thus, sex) in bdelloid rotifers, and no strong predicted evolutionary signatures of asexuality in TE dynamics in these species. Additionally, they find evidence for expansion of RNAi-related genes, which may play a role in countering the expected TE dynamics in asexual species. Overall, this work is substantial, thorough, and presents some answers to long-standing questions about the genome evolution of long-term asexual species.

  6. Version published to 10.1101/2020.09.15.297952v1 on bioRxiv
  7. Version published to 10.1101/2020.09.15.297952v2 on bioRxiv