Evidence for Ancient Asexuality in Bdelloid Rotifers

Welch and Meselson (2000) studied four genes, chosen because they are highly conserved and had been found in only a single copy in metazoan genomes; most results came from hsp82, which codes for an 82-kD heat shock protein. In rotifers that reproduce sexually, they found the usual pattern, in which the two homologous copies of each gene differ only slightly (on average, by 1% at fourfold degenerate sites; Fig. WN23.6A). However, within bdelloid individuals, copies showed extreme sequence divergence. For example, individuals of M. quadricornifera each contained two copies of hsp82 that differed by 54% at fourfold-degenerate sites (Fig. WN23.6B).

This pattern is expected, because as soon as asexual reproduction is established, the two copies of each gene in the ancestral diploid are propagated as separate lineages and accumulate mutations at neutral sites (Fig. WN23.6C). Thus, divergence between the two copies will be greater than between species that diverged since asexuality arose. This is just what is seen in the relationship among hsp82 genes from several asexual species of bdelloids and a sexual outgroup (Fig. WN23.6D). In some cases, more than two distinct copies were found; for example, P. roseola has four distinct versions of hsp82 (Pr1–4 in Fig. WN23.6D). This is due to a gene duplication, possibly due to polyploidization, that occurred in the ancestry of this species (Fig. WN23.6E).

However, recent work suggests that bdelloid rotifers arose as tetraploids. Although many exta gene copies have been lost, many genes are found in two pairs. The pairs are highly divergent (evidence originally interpreted as divergence between two copies in a diploid, expected with asexuality), but there is occasional gene conversion between the genes within each pair (Welch et al. 2008). These genetic data are consistent with ancient asexuality, but do not rule out occasional sexual reproduction between different individuals.

The unusual genomes of bdelloid rotifers may be a result of their extreme resistance to desiccation. These rotifers can resume reproduction after desiccation at any stage of their life cycle—adapting them to their life in ephemeral freshwater habitats. Desiccation causes extensive damage to DNA, which is efficiently repaired after rehydration. Thus, bdelloid rotifers also show extreme resistance to radiation (Gladyshev and Meselson 2008)—just like the desiccation-resistant bacterium, Deinococcus radiodurans (pp. 143 and 157). Repair of double-stranded breaks depends on copying information across from intact homologous chromosomes. This would explain why pairs of homologous chromosomes have been maintained for millions of years, apparently in the absence of sexual reproduction.