Evidence for Inefficient Selection Against Deleterious Mutations in Cytochrome Oxidase I of Asexual Bdelloid Rotifers

Abstract

Evolutionary theory predicts that natural selection should be less efficient in asexually than in sexually reproducing organisms. Obligate asexuals are expected to adapt slowly to changing environments and to accumulate mildly deleterious mutations to their genomes, potentially explaining their typically short evolutionary lifespans. One group of animals that appear to challenge these ideas is the bdelloid rotifers, a large and ancient clade of obligate asexuals. Previous work has found no evidence for inefficient selection against deleterious mutations in protein-coding genes of bdelloids. However, these studies relied mostly on between-species comparisons and were therefore unable to detect mildly deleterious mutations that persist within populations but are removed by selection over longer time periods. Here, we test for inefficient purifying selection acting on the cytochrome oxidase I (cox1) mitochondrial gene in 3 clades of bdelloids. Patterns of variation are compared to those of two facultatively sexual clades: a monogonont rotifer (Brachionus) and a branchiopod crustacean (Daphnia). As predicted due to the strict linkage between mitochondrial and nuclear genomes, bdelloids exhibit higher frequencies of putatively deleterious amino acid polymorphism within populations than the two facultatively sexual clades. While the monophyly and age of bdelloids makes it hard to rule out other explanations for the observed differences, several possible confounding factors, such as differences in effective population size or patterns of codon usage, are shown not to explain the observed differences. We therefore conclude that bdelloid mitochondrial DNA variation does display the signature of inefficient selection expected of obligate asexuals.

Long telomeres are associated with clonality in wild populations of the fissiparous starfish Coscinasterias tenuispina

“…Despite the fact that asexual reproduction facilitates clonal dispersion and renewal, it depends on mitotic divisions, which may increase the accumulation of somatic mutations, the Muller ratchet phenomena. Different studies with asexual species already revealed accumulation of somatic mutations on nonsynonymus position in clonal lineages compared with their nonclonal sibling species (Paland and Lynch, 2006;Barraclough et al, 2007). Unfortunately, the negative effects of deleterious mutations in wild populations of clonal species have never been fully investigated or proved, and these effects have been only supposed, but asexual lineages persist over short evolutionary periods (Schwander and Crespi, 2009).…”

The Effects of Deleterious Mutations on Evolution at Linked Sites

“…A recent study using population genetic data shows, however, that the effectiveness of selection on codon usage is greatly reduced in two different selfing species of plants compared with their outcrossing relatives (Qiu et al 2011). Similarly, the efficacy of selection on nonsynonymous mutations is higher in the outcrossing plant Capsella grandiflora than in the related selfer A. thaliana (Slotte et al 2010); in outcrossing vs. selfing species of Neurospora (Nygren et al 2011); and in sexual vs. asexual lineages of Daphnia (Paland and Lynch 2006), freshwater snails (Johnson and Howard 2007), and rotifers (Barraclough et al 2007). We are, however, far from having a comprehensive picture of the consequences of evolving low or zero rates of recombination throughout the genome.…”

How does the "ancient" asexual Philodina roseola (Rotifera: Bdelloidea) handle potential UVB-induced mutations?

“…Whereas older studies indicated that bdelloids have not accumulated slightly deleterious 54 mutations faster than facultative sexual monogonont rotifers (Welch and Meselson, 2001;55 Birky et al, 2005), two newer studies using more elaborate and extensive sampling strategies 56 indicated the possible existence of this effect (Barraclough et al, 2007;Swanstrom et al, 57 2011). However, the results of these latter studies, which examine the rate of historical 58 accumulation of deleterious mutations, are complicated by several confounding factors.…”

“…For 59 instance, the latest study showed no increased accumulation in bdelloid rotifers when 60 comparisons were made between monogononts and bdelloids from the same habitat 61 (Swanstrom et al, 2011). Additional potential confounding factors include methodological 62 aspects (e.g., sample-size effects (Swanstrom et al, 2011)), the long divergence time 63 separating bdelloids and monogononts (Barraclough et al, 2007), natural factors (e.g., 64…”

“…severely deleterious mutations that will not go to fixation (Barraclough et al, 2007)), and the 65 frequency and impact of any repair/recombination events (i.e., desiccation in bdelloids, sex in 66 monogononts). These difficulties notwithstanding, the long-term existence of bdelloids as a 67 group (at least 40 million years; (Ricci and Fontaneto, 2009)) would indicate that some 68 mechanism(s) to prevent genome degradation is present in these animals.…”