Bdelloid rotifers were believed to have persisted and diversified in the absence of sex. Two papers now show they exchange genes with each other, via horizontal gene transfers as known in bacteria and/or via other forms of non-canonical sex.

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1 Heethoff M.

Norton R.A.

Scheu S.

Maraun M. Parthenogenesis in oribatid mites (Acari, Oribatida): evolution without sex. 2 Schön I.

Rossetti G.

Martens K. Darwinulid ostracods: ancient asexual scandals or scandalous gossip?. 3 Mark Welch D.B.

Ricci C.

Meselson M. Bdelloid rotifers: progress in understanding the success of an evolutionary scandal. 2 Schön I.

Rossetti G.

Martens K. Darwinulid ostracods: ancient asexual scandals or scandalous gossip?. 4 Judson O.P.

Normark B.B. Ancient asexual scandals. 5 Butlin R. The costs and benefits of sex: new insights from old asexual lineages. Figure 1 Bdelloid rotifers. Show full caption 7 Ricci C.N. Ecology of bdelloids: how to be successful. Bdelloid rotifers are abundant, ubiquitous microinvertebrates that inhabit aqueous habitats. Depicted is an individual of the species Rotaria tardigrada. Picture courtesy of Michael Plewka ( http://www.plingfactory.de ). Asexual organisms are believed to be evolutionarily short-lived. Most asexual lineages occur on the tips of the tree of life and few have succeeded like their sexual counterparts. Only a handful of asexual lineages have diversified into different types considered as ‘species’ — sets of morphologically and ecologically distinct forms classified into different genera, or even families, of exclusively asexual organisms. The most prominent examples of lineages that have persisted and diversified over millions of years in the absence of sex include oribatid mites [], darwinulid ostracods [] (a group of freshwater Crustaceans) and, up to now, bdelloid rotifers [] ( Figure 1 ). These lineages have been referred to as ‘ancient asexual scandals’ as they appear to challenge the view that sex is a prerequisite for the long-term evolutionary success of a lineage []. They have also been considered a ‘holy grail’ for developing insights into one of the most notorious unresolved questions in evolutionary biology: why is sexual reproduction so universally favored in natural populations? The idea is that if we can understand how ancient asexual scandals persisted and diversified in the absence of sex, we might develop insights into what the most fundamental benefits of sex are [].

6 Debortoli N.

Li X.

Eyres I.

Fontaneto D.

Hespeels B.

Tang C.Q.

Flot J.-F.

Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. A new study in this issue of Current Biology by Debortoli et al. [] shows that the answer to how bdelloid rotifers have persisted and diversified in the absence of sex might be that bdelloids engage in an unusual form of ‘parasex’ that allows for horizontal genetic exchange between individuals in the absence of regular meiosis and the production of gametes. The mechanisms mediating these horizontal gene transfers between individuals remain unknown. But the phenotype, horizontal gene transfer, brings an outstanding example of convergent evolution between bacteria and eukaryotes. Furthermore, elucidating the molecular details of horizontal gene transfer in bdelloids may open novel avenues to large-scale genome editing.

7 Ricci C.N. Ecology of bdelloids: how to be successful. 8 Segers H. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. 9 Fontaneto D.

Herniou E.A.

Boschetti C.

Caprioli M.

Melone G.

Ricci C.

Barraclough T.G. Independently evolving species in asexual bdelloid rotifers. 7 Ricci C.N. Ecology of bdelloids: how to be successful. 10 Gladyshev E.A.

Meselson M.

Arkhipova I.R. Massive horizontal gene transfer in bdelloid rotifers. 11 Boschetti C.

Carr A.

Crisp A.

Eyres I.

Wang-Koh Y.

Lubzens E.

Barraclough T.G.

Micklem G.

Tunnacliffe A. Biochemical diversification through foreign gene expression in bdelloid rotifers. 12 Flot J.-F.

Hespeels B.

Li X.

Noel B.

Arkhipova I.

Danchin E.G.J.

Hejnol A.

Henrissat B.

Koszul R.

Aury J.-M.

et al. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. 13 Eyres I.

Boschetti C.

Crisp A.

Smith T.P.

Fontaneto D.

Tunnacliffe A.

Barraclough T.G. Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. Bdelloid rotifers are abundant micro-invertebrates that occur in aqueous habitats throughout the world []. There are 461 described species, distinguished from each other mainly on the basis of morphology []. Many species are able to survive dry, harsh conditions by entering a desiccation-induced state of dormancy from which they can emerge upon re-hydration []. The first hint for horizontal gene transfers in bdelloid rotifers was published in 2008 when Gladyshev and colleagues showed that bdelloid genomes harbor unusually many genes of bacterial, fungal, and plant origin []. Later work in the species Adineta ricciae then demonstrated that many of these foreign genes are expressed, and that as many as 8–10 % of all transcripts are of foreign origin []. The publication of the genome of a related species, Adineta vaga [], revealed a similar level of foreign gene content, with 8 % of predicted genes of non-metazoan origin. Finally, foreign gene uptake is ongoing in bdelloids and has contributed to functional differences among species [] and therefore to adaptive evolution in bdelloids.

14 Signorovitch A.

Hur J.

Gladyshev E.

Meselson M. Allele sharing and evidence for sexuality in a mitochondrial clade of bdelloid rotifers. 6 Debortoli N.

Li X.

Eyres I.

Fontaneto D.

Hespeels B.

Tang C.Q.

Flot J.-F.

Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Given the evidence that bdelloid rotifers acquire and use genes from non-metazoans, it seemed more than likely that horizontal gene transfers would also occur between bdelloid individuals and perhaps provide an alternative form of sex. The first evidence that bdelloids do indeed exchange genes with each other was provided by Signorovitch et al.[], who identified a pattern of allele sharing between individuals of the species Macrotrachela quadricornifera that was incompatible with strict asexual reproduction. In this issue of Current Biology, Debortoli et al. [] now provide additional evidence for genetic exchange between individuals without canonical sex in the species Adineta vaga. In combination, these two studies show beyond doubt that genetic exchange between individuals occurs in different bdelloid species and in different regions of the genome.

14 Signorovitch A.

Hur J.

Gladyshev E.

Meselson M. Allele sharing and evidence for sexuality in a mitochondrial clade of bdelloid rotifers. 15 Cleland R.E. Oenothera: Cytogenetics and Evolution. 16 Golczyk H.

Massouh A.

Greiner S. Translocations of chromosome end-segments and facultative heterochromatin promote meiotic ring formation in evening primroses. 17 Umen J.G. Lost and found: the secret sex lives of bdelloid rotifers. 12 Flot J.-F.

Hespeels B.

Li X.

Noel B.

Arkhipova I.

Danchin E.G.J.

Hejnol A.

Henrissat B.

Koszul R.

Aury J.-M.

et al. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. 6 Debortoli N.

Li X.

Eyres I.

Fontaneto D.

Hespeels B.

Tang C.Q.

Flot J.-F.

Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. 6 Debortoli N.

Li X.

Eyres I.

Fontaneto D.

Hespeels B.

Tang C.Q.

Flot J.-F.

Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Both papers thus provide direct evidence for some form of genetic exchange between bdelloid rotifer individuals. They disagree, however, as to how such genetic exchange occurs. Signorovitch et al. [] suggest that the patterns of allele sharing are best explained by extremely rare sexual reproduction involving an unusual form of chromosomal rearrangements found in some evening primroses of the genus Oenothera. These rearrangements, referred to as permanent translocation heterozygosity (PTH), result in chromosomes organized into a ring during meiosis and restrict recombination to the chromosome tips []. While there is currently no evidence for PTH in bdelloid rotifers, the proposed mechanism would be compatible with the highly rearranged genome structure characterizing bdelloids, which is incompatible with canonical forms of meiosis and sexual reproduction []. By contrast, Debortoli et al. [] suggest that allele sharing patterns in bdelloids are best explained by the same mechanism of horizontal gene transfers that led to the high proportion of foreign genes in the rotifer genomes. How these horizontal gene transfers generate allelic replacements, rather than genome expansions via the addition of horizontally acquired genes to the core genome, remains unclear and opens extraordinary avenues for future research directions. Another interesting open question is linked to the finding by Debortoli and colleagues [] that there is more extensive allele sharing between individuals within cryptic species than between individuals of different cryptic species of A. vaga. This finding indicates that horizontal gene transfer does not occur at random between individuals, but the mechanisms mediating these non-random gene exchanges remain unknown.

The two proposed mechanisms underlying allelic exchange between bdelloids, although not mutually exclusive, should generate different genome-wide patterns of divergence between rotifer individuals and species. For example, PTH would predict decreased divergence levels at chromosome tips relative to the genome-level average while horizontally acquired genes might a priori be scattered randomly across the genome. However, the currently available data do not allow to formally confirm or exclude the hypothesis of PTH in bdelloid rotifers, or to ascertain that the documented allele exchanges among bdelloid individuals solely stem from horizontal gene transfers.