Why most eukaryotes reproduce sexually has long been a major problem in evolutionary biology. After all, by not having to produce males, species that reproduce parthenogenetically should have a two-fold reproductive advantage over sexuals. Although there are several non-exclusive hypotheses for why sex predominates, all of them have been challenged until now by the apparent existence of a highly successful class of animals that arose tens of millions of years ago and which has long been thought to be entirely asexual—the rotifers of Class Bdelloidea.
As described in the February issue of the journal Genetics (PDF), Matthew Meselson and his associates have found clear genomic evidence that bdelloid rotifers do, after all, reproduce sexually, although only occasionally.
Bdelloid rotifers are tiny freshwater invertebrates that have fascinated biologists since Leeuwenhoek first described seeing them with his rudimentary microscope in 1677. Bdelloids are extremophiles, able to survive desiccation, starvation, extremes of temperature, and high doses of ionizing radiation. Despite much subsequent study in the laboratory and in the field, there has been no documented observation of bdelloid males. Until now, the prevailing view has therefore been that bdelloids are entirely asexual, although possibly exchanging genes by homologous horizontal gene transfer.
The new study focuses on three bdelloid strains designated MA, MM, and CR, all belonging to the species Macrotrachela quadricornifera. These strains were collected by the Meselson Lab 11 years ago at sites spread across the Northeastern US and have been reproducing asexually in the lab ever since.
Using a combination of 10x and Nanopore sequencing, Meselson and colleagues found that MA and MM identically share 1/4 of their genomes in the form of long segments in regions where one homolog of MA is identical to a homolog of MM, a situation known a “allele sharing”. Also, MA and MM both identically share 1/32 of their genomes with CR. The amount of MA-MM allele sharing and their equal distance from CR indicate that MA and MM are half-siblings or double first-cousins from a sexually reproducing population.
Some researchers have proposed that bdelloid rotifers exchange genetic material asexually, through homologous horizontal gene transfer (HGT), but such HGT has never been demonstrated, would be exceedingly unlikely to produce the observed pattern of allele sharing, and is unable to explain the entire absence of genomic regions in which sharing has occurred in both homologs at the same site.
In order to explain how the close relatives MA and MM could be found in their small sample (29 individuals selected as belonging to the same morphospecies) of what must be an enormous population, Meselson speculates that bdelloid males are produced and sexual reproduction occurs only in occasional “blooms” in bodies of water large enough that at least two genetically different but compatible lines are present together, giving rise to a large population of recombinants followed by wide dispersion and extensive clonal reproduction while lines that fail to outcross die out, as do asexual lines of other species.
Four different approaches were used to estimate when the sexual outcrossing event that produced MA and MM occurred. All four estimates agree that the observed genetic exchange occurred a few hundred to about a thousand bdelloid generations ago. As such blooms have never been carefully examined for male bdelloids, the suggestion is that doing so may at last reveal the elusive bdelloid males.
by Diana Crow and Matthew Meselson
