Rates of nucleotide substitution in sexual and anciently asexual rotifers

Abstract

The class Bdelloidea of the phylum Rotifera is the largest well studied eukaryotic taxon in which males and meiosis are unknown, and the only one for which these indications of ancient asexuality are supported by cytological and molecular genetic evidence. We estimated the rates of synonymous and nonsynonymous substitutions in the hsp82 heat shock gene in bdelloids and in facultatively sexual rotifers of the class Monogononta, employing distance based and maximum likelihood methods. Relative-rate tests, using acanthocephalan rotifers as an outgroup, showed slightly higher rates of nonsynonymous substitution and slightly lower rates of synonymous substitution in bdelloids as compared with monogononts. The opposite trend, however, was seen in intraclass pairwise comparisons. If, as it seems, bdelloids have evolved asexually, an equality of bdelloid and monogonont substitution rates would suggest that the maintenance of sexual reproduction in monogononts is not attributable to an effect of sexual reproduction in limiting the load of deleterious nucleotide substitutions.

Figure 1

Three-taxon tree used in relative-rate tests. The designations B, M, A, and O represent bdelloids, monogononts, acanthocephalans, and the common bdelloid-monogonont ancestor, respectively.

Figure 2

Scatter plot of unadjusted distances OB (bdelloids) and OM (monogononts) between the common bdelloid-monogonont ancestor and bdelloids or monogononts, respectively, based on 4-fold degenerate differences (A) and amino acid differences (B). Each point is obtained by the method of relative-rate tests for an individual set of bdelloid, monogonont, and acanthocephalan hsp82 sequences, except that the B. plicatilis sequence was not used for calculations of substitution per 4-fold degenerate site.

Figure 3

Phylogenetic trees for hsp82 sequences, with branch lengths proportional to synonymous (A) and nonsynonymous (B) substitutions, as estimated by the maximum likelihood method of Goldman and Yang (46). Numbers after bdelloid species names designate particular copies of hsp82 (25). The outgroup Seison nebaliae is not shown.