Sexual Reproduction in Bdelloid Rotifers

ABSTRACTNearly all eukaryotes reproduce sexually, either constitutively or facultatively, and nearly all that are thought to be asexual arose recently from sexuals, suggesting that loss of sex leads to early extinction. In apparent exception, there are several groups of ancient origin that have been thought to be entirely asexual. Of these, the most extensively studied are the rotifers of Class Bdelloidea. Yet the evidence for their asexuality is entirely negative -- the failure to establish the existence of males or hermaphrodites. Nevertheless, there is a growing body of evidence that bdelloids do reproduce sexually, albeit rarely, retaining meiosis-associated genes and, in a limited study of allele sharing in the bdelloid Macrotrachela quadricornifera, displaying a pattern of genetic exchange indicating recent sexual reproduction. Here we present a much larger study of allele sharing in the same system, clearly showing the occurrence of sexual reproduction, thereby removing the principal challenge to the generalization that sexual reproduction is essential for long-term evolutionary success in eukaryotes. We also discuss the relation between bdelloid life history and population structure and a possible benefit of outcrossing in restoring beneficial genome-wide epistatic interactions disrupted by loss of heterozygosity.STATEMENT OF SIGNIFICANCEMany hypotheses have been advanced to explain why, despite its substantial costs, sexual reproduction is nearly universal in eukaryotes and why the loss of sex generally leads to early extinction--a major problem in current evolution theory. Posing a challenge to all such hypotheses are a few groups of ancient origin that have been thought to be entirely asexual. Of these, the most extensively studied are the rotifers of Class Bdelloidea. Here we show that a bdelloid species is facultatively sexual, removing what had been a long-standing challenge to hypotheses for the benefit of sex. We also suggest that genome-wide beneficial epistasis may contribute to the advantage of sex over asex in diploids and to the predominance of diploidy over haploidy in eukaryotes.