Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Abstract

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years 1 . Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing 2 . However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873) 3 , and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.With more than 460 described species 4 , bdelloid rotifers ( Fig. 1) represent the highest metazoan taxonomic rank in which males, hermaphrodites and meiosis are unknown. Such persistence and diversification of an ameiotic clade of animals are in contradiction with the supposed long-term disadvantages of asexuality, making bdelloids an 'evolutionary scandal' 5 . Another unusual feature of bdelloid rotifers is their extreme resistance to desiccation at any stage of their life cycle 6 , enabling these microscopic animals to dwell in ephemeral freshwater habitats such as mosses, lichens and forest litter; this ability is presumably the source of their extreme resistance to ionizing radiation 7 .We assembled the genome of a clonal A. vaga lineage into separate haplotypes with a N 50 of 260 kilobases (kb) (that is, half of the assembly was composed of fragments longer than 260 kb). Assembly size was 218 megabases (Mb) but 26 Mb of the sequence had twice the average sequencing coverage, suggesting that some nearly identical regions were not resolved during assembly ( Supplementary Fig. 3); hence, the total genome size is likely to be 244 Mb, which corresponds to the estimate obtained independently using fluorometry (Supplementary Note C2). Annotation of the complete assembly (including all haplotypes) yielded 49,300 genes. Intragenomic sequence comparisons revealed numerous homologous blocks with conserved gene order (colinear regions). For each such block we computed the per-site synonymous d...

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…On the other hand, it has been proposed that desiccation and rehydration periods can induce a transient competence state for DNA uptake in the gut cells, permitting the acquisition of foreign DNA in the form of food particles or free DNA absorbed in mineral surfaces [20,23]. The immediate rspb.royalsocietypublishing.org Proc.…”

“…This study shows that around 10% of genes in the transcriptome of this species are of foreign origin and that 533 organisms could have contributed to the bdelloid genome as sources of horizontal gene transfer. The second study [23], dealing with the analysis of the Adineta vaga genome reveals the presence of 8% of foreign genes in this species, showing evidence of both ancient and recent transfers. Interestingly, glycosil hydrolases genes account for an important fraction of these presumptive transferred genes.…”

L’apophénie d’ENCODE ou Pangloss examine le génome humain

“…Alors qu'il y a un avantage pour une femelle à éliminer la production de mâle et à ne produire que des femelles, chez les eucaryotes la reproduction sexuée est la norme et la reproduction asexuée l'exception [35]. La distribution phylogénétique des organismes asexués indique que ceux-ci apparaissent régulièrement, mais qu'ils ne se maintiennent pas sur le long terme, même si quelques rares contre-exemples existent [36,37]. Des arguments théoriques et expérimentaux suggèrent que les organismes asexués ont une adaptabilité réduite du fait de la perte de la recombinaison qui permet la combinaison d'allèles favorables et l'élimination d'allèles délétères.…”

What can we infer about the origin of sex in early eukaryotes?

“…Genomic analysis shows the following: (i) the use of gene conversion, limiting the accumulation of mutations in the absence of meiosis; (ii) an increase of genes defending against transposons, with transposable elements being restricted to 3% of the genome; (iii) highly abundant horizontal gene transfer, 8% of genes probably having been obtained by this mechanism. An important conclusion in the light of the 'ROS-sex connection' proposed here: gene families involved in ROS resistance are strongly expanded as well [77]. To be able to survive desiccation, regularly occurring in their cyclically drying freshwater habitats, bdelloid rotifers evolved extraordinary resistance when confronted with ionizing radiation and concomitant ROS.…”

“…Real long-lived clonal eukaryotes, having irreversibly lost the option of meiotic sex, do exist however, and their characteristics strengthen the correlation between ROS and sex. Bdelloid rotifers, such as Adineta vaga, genome sequencing of which gave conclusive evidence for the absence of meiosis and sex, are the prime example [77]. These organisms have quite a lot to tell us.…”