Lost and Found: The Secret Sex Lives of Bdelloid Rotifers.

FIFTEEN years ago, Mark Welch and Meselson published a landmark paper that threw down a gauntlet to evolutionary biologists. They presented the first compelling molecular evidence that a large group of animals called bdelloid rotifers had been evolving for many millions of years without sex (Mark Welch and Meselson 2000). Their findings challenged the importance of sexual reproduction for long-term maintenance of a eukaryotic lineage and added considerable weight to the notion of asexual bdelloids as an evolutionary “scandal” (Smith 1986). Subsequent work by Meselson, Mark Welch, and colleagues uncovered an alternative explanation for their original findings based on the discovery that bdelloids are ancient tetraploids. Copies of genes that were originally interpreted as deeply diverged homologs that had ceased recombination were actually found to be homeologs that had most likely arisen from genome hybridization (Mark Welch et al. 2008). However, this finding did not rule out asexual evolution in bdelloids, in which among hundreds of cultured samples and natural populations, male bdelloids have not been observed (Birky 2010). Moreover, the case against sex in bdelloids received further support in a recent publication describing the sequencing of a bdelloid genome whose structure is incompatible with conventional meiosis (Flot et al. 2013). Instead of typical sets of homologous chromosomes, the tetraploid bdelloid genome is full of rearrangements and translocations that place some genes that were once allelic pairs on the same chromosome. Case closed for asexual evolution in bdelloids? Apparently not. In this issue of GENETICS, Meselson and co-workers report the surprising finding that bdelloids have a sex life after all—though clearly not a conventional one (Signorovitch et al. 2015). It is worth revisiting the reason why apparent loss of sexuality in bdelloids has been a conundrum for evolutionary biologists [though see Birky (2010) for an alternative view]. Sexual reproduction via meiosis (recombination and genome reduction) and syngamy (gamete fusion) is an ancient eukaryotic innovation (Goodenough and Heitman 2014), and its maintenance and near ubiquity speak to its importance. There are many reasons why sexual reproduction is thought to be beneficial and remains under long-term selection, not least of which are the efficiency with which deleterious alleles can be purged from a sexual population and the rapidity with which an adaptive landscape can be explored through the generation of sexual recombinants. Lineages that lose sex tend to adapt more slowly than sexual ones, and they may undergo genomic degeneration through the slow accumulation and fixation of deleterious mutations, a process known as Muller’s ratchet. In the short term, however, asexual (i.e., clonal) reproduction can be a highly successful means of propagating and expanding a population with a well-adapted genotype because clonal progeny do not suffer the cost of genomic reshuffling or the twofold cost of males that are associated with sex (Butlin 2002; Otto 2009). In the face of these opposing costs and benefits, eukaryotes have evolved a diverse range of reproductive strategies including obligately sexual (e.g., humans and many other animals), facultatively sexual (e.g., algae, fungi, and many unicellular eukaryotes), and completely asexual (e.g., dandelions). What distinguishes complete asexuals from the first Copyright © 2015 by the Genetics Society of America doi: 10.1534/genetics.115.176388 Address for correspondence: Donald Danforth Plant Science Center, 975 N. Warson Rd., St. Louis, MO 63132. E-mail: [email protected]