Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Abstract

The genome of the asexual rotifer Adineta vaga lacks homologous chromosomes; instead, its allelic regions are rearranged and sometimes found on the same chromosome in a palindromic fashion, a structure reminiscent of the primate Y chromosome and of other mitotic lineages such as cancer cells. Bdelloid rotifers are thought to have persisted and diversified asexually for millions of years, which is odd because loss of sexual reproduction is widely considered to be an evolutionary dead end for metazoans. The suspicion remained that they might engage in sex on rare occasions. But here Olivier Jaillon and colleagues sequence the genome of a bdelloid rotifer, Adineta vaga, and show that its structure is incompatible with conventional meiosis, the type of cell division associated with sexual reproduction. The genome has undergone abundant gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Up to 8% of the genes are of probable non-metazoan origin, probably acquired through horizontal gene transfer. These findings demonstrate positive evidence for asexual evolution, supporting the hypothesis of ancient asexuality among bdelloid rotifers. Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.