Sex brings transposons and genomes into conflict

Abstract

Given that transposons are so abundant in mammalian genomes, it is natural to assume that through their maintenance the host gains some net benefit. This need not be true; sexual reproduction allows a transposon to go to fixation if the reduction in fitness of the host is anything less than two-fold. Obligate outcrossing sexual reproduction therefore favors the evolution of aggressive transposons, which in turn select for the evolution of host mechanisms that suppress transposon activity. Hosts that have asexual or self-fertilizing generations will select for transposons that are more benign and self-limiting than those of obligate sexuals, and obligate asexuals and uniparental organelle genomes will be free of active transposons if these impose any fitness penalty. We are interested in host mechanisms that suppress transposons in sexuals and have found that mammals (all of which are obligate sexuals) control their large populations of potentially active retroposons by methylating the five position of cytosine residues within promoter elements. This causes strong transcriptional repression and assembly of the affected sequences into the condensed state. Methylation also causes permanent inactivation in the germline by driving C→T transition mutations at methylated sites. It is now known that methylation remains in place for the large majority of the life of germ cells and is essential for control of the very large transposon burden. There is pressure on transposons to evolve mechanisms that overcome host suppression, and over evolutionary time, the balance swings back and forth between parasite and host. The ability of the mammalian genome to absorb and accumulate additional transposons has caused the amount of reverse transcriptase coding sequence in the human genome to far exceed the sum total of all cellular coding sequence. While transposons could, in principle, contribute functions useful to the host, the fact that asexual species and uniparental organelle genomes lack transposons is strong evidence that transposons have a net deleterious effect even in genomes that might be thought to require an additional source of plasticity. The abundance of transposons in many genomes cannot be taken as evidence of a mutualistic relationship, and the conflict between transposons and genomes may have actually retarded rather than accelerated evolution. It is suggested that the relationship between sex and transposons is as follows: (i) Obligate sexuals will tend to harbor aggressive transposons limited largely by host suppressive mechanisms, which in mammals involve methylation of transposon promoters. (ii) The aggressiveness of transposons in facultative sexuals and self-fertilizing sexuals will be in part self-limited and will be proportional to the relative frequency of asexual and outcrossing sexual generations. (iii) Obligate asexuals and organelles transmitted in a uniparental manner will have no active transposons if these have a net negative effect on host fitness.