Genomic signature of sexual reproduction in the bdelloid rotifer Macrotrachella quadricornifera.

Bdelloid rotifers, common freshwater invertebrates of ancient origin and worldwide distribution have long been thought to be entirely asexual, being the principal exception to the view that in eukaryotes the loss of sex leads to early extinction. That bdelloids are facultatively sexual is shown by a study of allele sharing within a group of closely related bdelloids of the species Macrotrachella quadricornifera, supporting the view that sexual reproduction is essential for long-term success in all eukaryotes.

Evidence for meiotic sex in bdelloid rotifers.

In their study of genetic exchange in the bdelloid rotifer Adineta vaga, Debortoli et al. [1] conclude that the patchwork pattern of allele sharing among three individuals in the genomic regions they examined is "…unlikely to arise in cases of PTH (Oenothera-like) meiosis since haplotypes are transferred as entire blocks…" and therefore that "Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex." This assumes without justification that horizontal gene transfer (HGT) in bdelloids precludes the sexual transmission of entire haplotypes, for which we have reported evidence in the bdelloid Macrotrachela quadricornifera[2].

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers.

Rotifers of Class Bdelloidea are common freshwater invertebrates of ancient origin whose apparent asexuality has posed a challenge to the view that sexual reproduction is essential for long-term evolutionary success in eukaryotes and to hypotheses for the advantage of sex. The possibility nevertheless exists that bdelloids reproduce sexually under unknown or inadequately investigated conditions. Although certain methods of population genetics offer definitive means for detecting infrequent or atypical sex, they have not previously been applied to bdelloid rotifers.

The centenary of Janssens's chiasmatype theory.

The segregation and random assortment of characters observed by Mendel have their basis in the behavior of chromosomes in meiosis. But showing this actually to be the case requires a correct understanding of the meiotic behavior of chromosomes. This was achieved only gradually, over several decades, with much dispute and confusion along the way.

Extreme anti-oxidant protection against ionizing radiation in bdelloid rotifers.

Bdelloid rotifers, a class of freshwater invertebrates, are extraordinarily resistant to ionizing radiation (IR). Their radioresistance is not caused by reduced susceptibility to DNA double-strand breakage for IR makes double-strand breaks (DSBs) in bdelloids with essentially the same efficiency as in other species, regardless of radiosensitivity. Instead, we find that the bdelloid Adineta vaga is far more resistant to IR-induced protein carbonylation than is the much more radiosensitive nematode Caenorhabditis elegans.

Phylogenomics of unusual histone H2A Variants in Bdelloid rotifers.

Rotifers of Class Bdelloidea are remarkable in having evolved for millions of years, apparently without males and meiosis. In addition, they are unusually resistant to desiccation and ionizing radiation and are able to repair hundreds of radiation-induced DNA double-strand breaks per genome with little effect on viability or reproduction. Because specific histone H2A variants are involved in DSB repair and certain meiotic processes in other eukaryotes, we investigated the histone H2A genes and proteins of two bdelloid species.

Degenerate tetraploidy was established before bdelloid rotifer families diverged.

Rotifers of Class Bdelloidea are abundant freshwater invertebrates known for their remarkable ability to survive desiccation and their lack of males and meiosis. Sequencing and annotation of approximately 50-kb regions containing the four hsp82 heat shock genes of the bdelloid Philodina roseola, each located on a separate chromosome, have suggested that its genome is that of a degenerate tetraploid. In order to determine whether a similar structure exists in a bdelloid distantly related to P.

Massive horizontal gene transfer in bdelloid rotifers.

Horizontal gene transfer in metazoans has been documented in only a few species and is usually associated with endosymbiosis or parasitism. By contrast, in bdelloid rotifers we found many genes that appear to have originated in bacteria, fungi, and plants, concentrated in telomeric regions along with diverse mobile genetic elements. Bdelloid proximal gene-rich regions, however, appeared to lack foreign genes, thereby resembling those of model metazoan organisms.

Extreme resistance of bdelloid rotifers to ionizing radiation.

Rotifers of class Bdelloidea are common invertebrate animals with highly unusual characteristics, including apparently obligate asexuality, the ability to resume reproduction after desiccation at any life stage, and a paucity of transposable genetic elements of types not prone to horizontal transmission. We find that bdelloids are also extraordinarily resistant to ionizing radiation (IR). Reproduction of the bdelloids Adineta vaga and Philodina roseola is much more resistant to IR than that of Euchlanis dilatata, a rotifer belonging to the desiccation-intolerant and facultatively sexual class Monogononta, and all other animals for which we have found relevant data.

Evidence for degenerate tetraploidy in bdelloid rotifers.

Rotifers of class Bdelloidea have evolved for millions of years apparently without sexual reproduction. We have sequenced 45- to 70-kb regions surrounding the four copies of the hsp82 gene of the bdelloid rotifer Philodina roseola, each of which is on a separate chromosome. The four regions comprise two colinear gene-rich pairs with gene content, order, and orientation conserved within each pair.

A deep-branching clade of retrovirus-like retrotransposons in bdelloid rotifers.

Rotifers of class Bdelloidea, a group of aquatic invertebrates in which males and meiosis have never been documented, are also unusual in their lack of multicopy LINE-like and gypsy-like retrotransposons, groups inhabiting the genomes of nearly all other metazoans. Bdelloids do contain numerous DNA transposons, both intact and decayed, and domesticated Penelope-like retroelements Athena, concentrated at telomeric regions. Here we describe two LTR retrotransposons, each found at low copy number in a different bdelloid species, which define a clade different from previously known clades of LTR retrotransposons.

Diverse DNA transposons in rotifers of the class Bdelloidea.

We surveyed the diversity, structural organization, and patterns of evolution of DNA transposons in rotifers of the class Bdelloidea, a group of basal triploblast animals that appears to have evolved for millions of years without sexual reproduction. Representatives of five superfamilies were identified: ITm (IS630/Tc/mariner), hAT, piggyBac, helitron, and foldback. Except for mariners, no fully intact copies were found.

Deleterious transposable elements and the extinction of asexuals.

The genomes of virtually all sexually reproducing species contain transposable elements. Although active elements generally transpose more rapidly than they are inactivated by mutation or excision, their number can be kept in check by purifying selection if its effectiveness becomes disproportionately greater as their copy number increases. In sexually reproducing species, such synergistic selection can result from ectopic crossing-over or from homologous recombination under negative epistasis.

Divergent gene copies in the asexual class Bdelloidea (Rotifera) separated before the bdelloid radiation or within bdelloid families.

Rotifers of the asexual class Bdelloidea are unusual in possessing two or more divergent copies of every gene that has been examined. Phylogenetic analysis of the heat-shock gene hsp82 and the TATA-box-binding protein gene tbp in multiple bdelloid species suggested that for each gene, each copy belonged to one of two lineages that began to diverge before the bdelloid radiation. Such gene trees are consistent with the two lineages having descended from former alleles that began to diverge after meiotic segregation ceased or from subgenomes of an alloploid ancestor of the bdelloids.

Cytogenetic evidence for asexual evolution of bdelloid rotifers.

DNA sequencing has shown individual bdelloid rotifer genomes to contain two or more diverged copies of every gene examined and has revealed no closely similar copies. These and other findings are consistent with long-term asexual evolution of bdelloids. It is not entirely ruled out, however, that bdelloid genomes consist of previously undetected pairs of sequences so similar as to be identical over the regions sequenced, as might result if bdelloids were highly inbred sexual diploids or polyploids.

Retroelements containing introns in diverse invertebrate taxa.

We report that two structurally similar transposable elements containing reverse transcriptase (RT), Penelope in Drosophila virilis and Athena in bdelloid rotifers, have proliferated as copies containing introns. The ability of Penelope-like elements (PLEs) to retain introns, their separate phylogenetic placement and their peculiar structural features make them a novel class of eukaryotic retroelements.