Deleterious transposable elements and the extinction of asexuals

Abstract

The genomes of virtually all sexually reproducing species contain transposable elements. Although active elements generally transpose more rapidly than they are inactivated by mutation or excision, their number can be kept in check by purifying selection if its effectiveness becomes disproportionately greater as their copy number increases. In sexually reproducing species, such synergistic selection can result from ectopic crossing-over or from homologous recombination under negative epistasis. In addition, there may be controls on transposon activity that are associated with meiosis. Because a sexual lineage that abandons sex must lack such mechanisms, it may be driven to extinction by the unchecked proliferation of deleterious transposons inherited from its sexual progenitor. An important component of the evolutionary advantage of sex over asex may therefore lie in the ability of sex, despite facilitating the spread of deleterious elements within interbreeding populations, also to restrain their intragenomic proliferation.

Diverse DNA transposons in rotifers of the class Bdelloidea

“…Its short 5Ј and 3Ј noncoding regions comprise 133 and 74 bp, respectively. A TATA-like sequence, (TA) 5 , at position 86 is expanded to (TA) [6][7][8] in some copies.…”

“…An additional possibility dependent on sexual reproduction is recombination with synergistic epistasis, and, at least in some species and perhaps generally, there are silencing mechanisms associated with meiosis. Therefore, we have suggested that the absence of these various mechanisms in asexuals may lead to the unchecked intragenomic proliferation of retrotransposons and may be a major factor responsible for the relatively early extinction of lineages that abandon sexual reproduction and, correspondingly, for the advantage of sex over asex (6,7). In that case, ancient asexuals, if they exist, would be expected to lack intact transposable elements, except for those that are introduced by horizontal transmission or that serve some function advantageous to their host, and are subject to limiting mechanisms not dependent on sex.…”

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

“…Some theories predict that transposable elements should be either absent from the genomes of asexuals 18 or undergo unrestrained expansion after the switch to asexuality, potentially leading to species extinction unless transposable element proliferation is prevented 19 . We found that transposable elements cover about 3% of the A. vaga genome, which is less than the percentage reported in most other metazoans (including the genome of the obligate parthenogenetic nematode Meloidogyne incognita, 36% of which is made up of repetitive elements 20 ).…”

Double-strand breaks associated with repetitive DNA can reshape the genome

“…Although some CAs are selectively advantageous, there are also negative consequences to a mechanism that generates high rates of CAs. Selection against cells with high levels of genome instability, reflecting high levels of transposable elements, may be one mechanism by which the number of such elements per genome is limited (32). In higher eukaryotes such as humans, whose genomes are replete with repetitive DNA, a compromise between opportunities for variation and excessive genome instability could be accomplished by increasing the efficiency of local interactions (end rejoining and sister chromatid recombination) and by shifting the balance of DSB repair from homologous to nonhomologous pathways.…”